Review ArticleFungal Laccases and Their Applications in Bioremediation

Buddolla Viswanath Bandi Rajesh Avilala JanardhanArthala Praveen Kumar and Golla Narasimha

Applied Microbiology Laboratory Department of Virology Sri Venkateswara University Tirupati 517 502 India

Correspondence should be addressed to Buddolla Viswanath buddollagmailcomand Golla Narasimha gnsimha123rediffmailcom

Received 13 November 2013 Accepted 22 April 2014 Published 15 May 2014

Academic Editor David Ballou

Copyright copy 2014 Buddolla Viswanath et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Laccases are blue multicopper oxidases which catalyze the monoelectronic oxidation of a broad spectrum of substrates forexample ortho- and para-diphenols polyphenols aminophenols and aromatic or aliphatic amines coupled with a full four-electron reduction of O

2to H2O Hence they are capable of degrading lignin and are present abundantly in many white-rot

fungi Laccases decolorize and detoxify the industrial effluents and help in wastewater treatment They act on both phenolic andnonphenolic lignin-related compounds as well as highly recalcitrant environmental pollutants and they can be effectively used inpaper and pulp industries textile industries xenobiotic degradation and bioremediation and act as biosensors Recently laccasehas been applied to nanobiotechnology which is an increasing research field and catalyzes electron transfer reactions withoutadditional cofactors Several techniques have been developed for the immobilization of biomolecule such as micropatterning self-assembledmonolayer and layer-by-layer techniques which immobilize laccase and preserve their enzymatic activity In this reviewwe describe the fungal source of laccases and their application in environment protection

1 Introduction

Fungi can exploit marginal living conditions in large partbecause they produce unusual enzymes capable of perform-ing chemically difficult reactions [1 2] Interest in laccaseshas increased recently because of their potential use in thedetoxification of pollutants and in bioremediation of phe-nolic compounds [3ndash5] These fungal enzymes can convertwood plastic paint and jet fuel among other materialsinto nutrients Some of these enzymes have already beenharnessed in pulp and paper processing and in the synthesisof fine chemicals [6] Recent studies have suggested thatlignin-degrading or white-rot fungi (decay caused by thesespecies that gives wood a bleached appearance) such asPhanerochaete chrysosporium and Trametes versicolor couldreplace some of the chemical steps used in paper making[2 7]

The use of enzymes for the treatment or the removal ofenvironmental and industrial pollutants has attracted incre-

asing attention because of their high efficiency high selectiv-ity and environmentally benign reactions Of these enzymesstudied for such purposes extracellular fungal peroxidasessuch as lignin peroxidase manganese peroxidase and fungallaccases are the two major classes of enzymes that have beenevaluated for the removal of toxic phenolic compounds fromindustrial wastewater and the degradation of recalcitrantxenobiotics Numerous reports have been published recentlyon the improvements of the production of these enzymessuch as discovery of new fungal strains modification ofgrowth conditions use of inducers and use of cheaper growthsubstrates such as agricultural and food wastes The reviewof the literature given below is therefore an account relatingto laccases and their production purification biochemicalcharacterization and their applications

Laccase (EC 11032 p-diphenol dioxygen oxidoreduc-tase) is one of a few enzymes that have been studied sincethe nineteenth century Yoshida first described laccase in 1883whenhe extracted it from the exudates of the Japanese lacquer

Hindawi Publishing CorporationEnzyme ResearchVolume 2014 Article ID 163242 21 pageshttpdxdoiorg1011552014163242

2 Enzyme Research

tree Rhus vernicifera [8] In 1896 laccase was demonstratedto be a fungal enzyme for the first time by both Bertrand andLaborde [9] Laccases of fungi attract considerable attentiondue to their possible involvement in the transformation of awide variety of phenolic compounds including the polymericlignin and humic substances [10] Most lignolytic fungalspecies produce constitutively at least one laccase isoenzymeand laccases are also dominant among lignolytic enzymes inthe soil environment In addition laccase-mediated deligni-fication allows increasing the nutritional value of agroindus-trial byproducts for animal feed or soil fertilizer [11]

The fact that they only require molecular oxygen forcatalysis makes them suitable for biotechnological applica-tions for the transformation or immobilization of xenobioticcompounds [12] The major role of laccases in lignin andphenolic compound degradation has been evaluated in alarge number of biotechnological applications such as dyedegradation bioremediation of some toxic chemical wastes(eg chlorinated aromatic compounds polycyclic aromatichydrocarbons nitroaromatics and pesticides) and biosensordevelopments [11ndash13] Commercially laccases have been usedto delignify wood tissues produce ethanol and distinguishbetween morphine and codeine Research in recent yearshas been intense much of it elicited by the wide variety oflaccases their utility and their very interesting propertiesThe current status of knowledge with regard to fungal laccaseand their applications to protect environment is reviewed

2 Distribution and PhysiologicalFunctions of Laccases

Laccases are common enzymes in nature and are foundwidely in plants and fungi as well as in some bacteria andinsects [14]The physiological functions of these biocatalystswhich can be secreted or intracellular are different in thevarious organisms but they all catalyse polymerization ordepolymerization processes [15] As mentioned earlier thefirst laccase was reported in 1883 from Rhus vernicifera theJapanese lacquer tree from which the designation laccasewas derived and the enzyme was characterized as a metalcontaining oxidase [16] This makes it one of the earliestenzymes ever described Laccases have subsequently beendiscovered from other numerous plants [17] but the detectionand purification of plant laccases are often difficult becausecrude plant extracts contain a large number of oxidativeenzymes with broad substrate specificities [17] which isprobably the reason why detailed information about thebiochemical properties of plant laccase is limited HoweverRhus vernicifera laccase is an exception and has been exten-sively studied especially with regard to its spectroscopicproperties [18] R vernicifera laccase has also widely beenused in investigations of the general reaction mechanism oflaccases [19 20] Plant laccases are found in the xylem wherethey presumably oxidize monolignols in the early stages oflignification [21] and also participate in the radical-basedmechanisms of lignin polymer formation [22] In additionlaccases have been shown to be involved in the first steps ofhealing in wounded leaves [23] However the occurrence of

laccases in higher plants appears to be far more limited thanin fungi [24 25]

Only a few bacterial laccases have been described hith-ertoThe first bacterial laccase was detected in the plant root-associated bacterium ldquoAzospirillum lipoferumrdquo [26] whereit was shown to be involved in melanin formation [27]An atypical laccase containing six putative copper-bindingsites was discovered from Marinomonas mediterranea butno functional role has been assigned to this enzyme [28]Bacillus subtilis produces a thermostable CotA laccase whichparticipates in pigment production in the endospore coat[29] Laccases have also been found from Streptomyces cya-neus [30] and Streptomyces lavendulae [31] Although thereare also some other reports about laccase activity in bacteriait does not seem probable that laccases are common enzymesfrom certain prokaryotic groups [32] Bacterial laccase-likeproteins are intracellular or periplasmic protein [10] Laccasesproducing bacteria from different environmental sourceswith their possible physiological functions of laccase aregiven below B licheniformis is a novel melanogenic soilbacterium isolated from soil which protects strain from UVlight and the oxidants [33] It is involved in dimerization ofphenolic acids [34] Bacillus endospores producing laccasewere isolated from soil and the enzyme involved in phenoldegradation [5 35]

Laccase activity has been demonstrated in many fun-gal species belonging to ascomycetes and basidiomycetesand the enzyme has already been purified from manyspecies There are many records of laccase production byascomycetes Phytopathogenic ascomycetes like Melanocar-pus albomyces [36]Cerrena unicolor [37]Magnaporthe grisea[38] Trametes versicolor [14] Trichoderma reesei [39] andXylaria polymorpha [40]are examples for laccase productionand the enzyme was purified Besides in plant pathogenicspecies laccase production was also reported for some soilascomycete species from the genera Aspergillus Curvulariaand Penicillium [41] as well as some fresh water ascomycetes[42] Yeasts are a physiologically specific group of bothascomycetes and basidiomycetes Until now laccase wasonly purified from the human yeast pathogen Cryptococcus(Filobasidiella) neoformans This yeast produces true laccasecapable of oxidation of phenols and aminophenols andunable to oxidize tyrosine [43] The enzyme is tightly boundto the cell wall and contributes to the resistance to fungicides[44] Among physiological groups of fungi laccases are typ-ical of the wood-rotting basidiomycetes which cause whiterot and a related group of litter-decomposing saprotrophicfungi that is the species causing lignin degradation Almostall species of white-rot fungi were reported to produce laccasein varying degrees and the enzyme has been purified frommany species [45]

The majority of laccases characterized so far have beenderived from white-rot fungi which are efficient lignin deg-raders [46] Many fungi contain several laccase-encodinggenes but their biological roles are mostly not well under-stood [47] Agaricus bisporus [48] Botrytis cinerea [49]Coprinus cinereus [50] Phlebia radiata [51] Pleurotus ostrea-tus [52] and Trametes versicolor [53] were some examplesof basidiomycetes that produce laccases In addition to

Enzyme Research 3

plants bacteria and fungi laccases or laccase-like activitieshave been found in some insects where they have beensuggested to be active in cuticle sclerotization [54] Recentlylaccases have been represented as candidates for ligninmodification enzymes (ldquolignasesrdquo) in termites Predominantlaccase activities against DMP and ABTS were detected inthe fungus combs and fungi isolated from the nests of threegenera of fungus-growing termites that is MacrotermesOdontotermes andMicrotermes [55ndash57]

3 Screening of Fungal Species

Screening of laccase producing fungal species and theirvariants is important for selecting suitable laccase producingorganisms For this reason one usually relies on the use ofinexpensive rapid and sensitive testingmethodsThe screen-ing strategy must aim to identify fungal strains and enzymesthat will work under industrial conditions [58] Discoveryof novel laccases with different substrate specificities andimproved stabilities is important for industrial applicationsFungi that produce laccase have been screened for eitheron solid media containing coloured indicator compoundsthat facilitate the visual detection of laccase production[59] or with liquid cultivations monitored with enzymeactivity measurements [60] The use of coloured indicatorsis generally simpler as no sample handling and measurementare required As laccases oxidize various types of substratesseveral different compounds have been used as indicators forlaccase production

The traditional screening reagents tannic acid and gallicacid [61] have nowadays mostly been replaced with synthe-tic phenolic reagents such as guaiacol and syringaldazine[59 62] or with the polymeric dyes Remazol Brilliant BlueR (RBRR) and Poly R-478 [63] RBRR and Poly R-478are decolourized by lignin degrading fungi [64] and theproduction of laccase is observed as a colourless halo aroundmicrobial growth With guaiacol a positive reaction is indi-cated by the formation of a reddish brown halo [59] whilewith the tannic acid and gallic acid the positive reaction is adark-brown coloured zone [61] Kiiskinen et al [46] screenednovel laccase producing fungi by a plate method based onpolymeric dye compounds guaiacol and tannic acid

4 Cultural and NutritionalConditions for Laccase Production

Culture conditions and medium composition play a majorrole in enzyme expression Laccase production by fungi isstrongly affected by many fermentation parameters such astime of cultivation stationary or submerged cultures organicor inorganic compound concentrations inducer concentra-tion [65] aeration [66] and degradation or activation byprotease [67] Laccases are generally produced during thesecondary metabolism of white-rot fungi growing on naturalsubstrate or in submerged culture [2] Physiological demandsvary among white-rot fungi and considerable research hasbeen done on the influence of agitation pH temperaturecarbon nitrogen sources andmicroelements and their levels

Dong et al [68] compared laccase production byTrametesgallica on twelve media under static or shaking conditionsThey concluded that twelve culture media in addition tostatic and shaking conditions show great influence onamount and pattern of laccase isoenzymes from Trametesgallica Gayazov and Rodakiewicz-Nowak [69] reportedfaster laccase production under semicontinuous cultivationwith high aeration and culture mixing compared to staticconditionsWhenusing conical flasks for cultivation it shouldbe baffled to ensure a high oxygen transfer [70] Simi-larly Piscitelli et al [71] described the influence of variousphysiological factors on laccase formation in a number ofwhite-rot fungi Refined media are necessary for obtaininglarge amount of laccases that may be used in biochemicalanalysis and industrial application Extracellular laccases ofwhite-rot fungi exist in isozymes that may be inducible orconstitutive Ganoderma lucidum produced more than threelaccase isozymes in liquid culture [72] Pleurotus pulmonariusproduced three laccase isozymes among which the lcc1 andlcc2 isoforms were produced in noninduced cultures whilelcc3 was found only in induced-culture filtrates [73] At leastseven laccase isozymes were found in the basidiomyceteCECT 20197 [74]Three constitutive and four induced laccaseisozymes were found in Marasmius querocophilus strain17 [75] At least nine constitutive laccase isozymes weredescribed for Pleurotus sp [76] The pattern of isozymes hasbeen successfully applied in the identification of a numberof different microorganisms particularly fungi such as ecto-mycorrhiza [77] deuteromycetes [78] and basidiomycetes[79 80]

A common technique for comparison of isozyme patternsfrom different sources is the use of zymograms [81] Praveenet al [82] found that the production of high titres of thelaccase enzyme was not dependent on high biomass yieldsBut laccase production was found to be highly related to theconditions of cultivation of the fungus [82 83] and mediasupporting high biomass did not necessarily support highlaccase yields [84] The synthesis and activity of the laccasewere controlled during growth and can play an importantrole in pigment and fruiting body formation [8 85] Buswellet al [86] reported that the production of laccase wasstrongly affected by the nature and amounts of nutrientsespecially nitrogen and trace elements in the growthmediumLaccases were generally produced in low concentrations bylaccase producing fungi [87] but higher concentrations wereobtainable with the addition of various supplements tomedia[71] Laccase production by Phanerochaete chrysosporiumwas not detected in low or high nitrogen medium withglucose as the carbon source but was produced when theorganism was grown on low or high nitrogen medium withcellulose as the carbon source [88] whereas in the white-rot fungus Ganoderma lucidum higher levels of laccaseswere produced in high nitrogen medium with glucose asthe carbon source [89] Ligninolytic systems of white-rotfungi were mainly activated during the secondary metabolicphase and were often triggered by nitrogen concentration[86] or when carbon or sulfur became limited [83] Theaddition of xenobiotic compounds such as xylidine lignin

4 Enzyme Research

and veratryl alcohol was known to increase and induce lac-case activity [84] Towards maximization of laccase secretionwith culture additives Sinegani et al [90] studied laccaseproduction by Aspergillus terreus Armillaria sp Polyporussp and Phanerochaete chrysosporium in liquid culture mediatreated with N-ethyl aniline NN-dimethyl aniline and para-bromoaniline as a laccase inducer

Optimization of the production medium plays a majorrole in higher laccase production The Taguchi approachof OA DOE constitutes a simple methodology that selectsthe best conditions producing consistent performance Thisapproach led to an increase in laccase yield to 820ULfrom 485UL The increased production of laccase wasalso confirmed by the dye decolorization experiment whichshowed an increased decolorization of reactive blue 221 from45 to 846 in the same unit volume [91]

41 Influence of pH on Laccase Production ThepHof the cul-ture medium is critical and plays a significant role in thegrowth and laccase production of the organism There isnot much information available on the influence of pH onlaccase production but when fungi are grown in a mediumwith pH 50 laccase will be produced in excess [8] Mostreports indicated initial pH levels set between pH 4 and6 prior to inoculation but the levels were not controlledduringmost cultivations [87 92]The optimumpH of laccaseproduction as reported in many fungi falls between 50and 60 [14 93 94] Maximum titres of laccase and biomasswere observed in the medium adjusted to pH 60 by Fomessclerodermeus white-rot basidiomycetes The optimal rangefor the laccase isoforms secreted by Trametes pubescensfungal strain has been reported between pH 30 and 45potentially indicating that laccase may be produced andfunction optimally under conditions that are not favourableto growth [95] Laccases from fungi have been found in wideapplications ranging from the pharmaceutical sector to thepulp and paper industry but eukaryotic laccases generallyprefer low pH for better functioning In contrast bacteriallaccases can act and are more stable at wider pH range[96 97] With the advantage of immense environmentaladaptability and biochemical versatility prokaryotes deserveto be studied for their possible applications in industry as wellas in medical science [5]

42 Influence of Temperature on Laccase Production Temper-ature like any other physical parameters plays a vital rolein growth and laccase production of the organism It hasbeen found that the optimal temperature for fruiting bodyformation and laccase production is 25∘C in the presence oflight but 30∘C for laccase production when the cultures areincubated in the dark [8] In general the fungi were cultivatedat temperatures between 25∘C and 30∘C for optimal laccaseproduction [14]When cultivated at temperatures higher than30∘C the activity of laccase was reduced [98] The wood-decaying basidiomycete Steccherinum ochraceum isolate 1833was reported to produce three highly thermostable laccaseisoforms with maximum activities in the region 75ndash80∘C[99 100] Therefore it is proved that optimum production oflaccase can differ greatly from one strain to another

43 Influence of Carbon on Laccase Production Carbon is apart of all living organisms Breakdown of carbon sourcesliberates energy which is utilized by the organism for growthand development The most readily usable carbon source bywhite-rot fungi is glucose [101] Collins and Dobson [102]reported that glucose at 10 gL enhanced the growth and lac-case production by Coriolus versicolor In Trametes versicolorglucose at higher concentration (20 gL) favoured laccaseproduction [14] In Ganoderma lucidum glucose at 20 gLincreased the mycelial growth but at 10 gL favoured expres-sion of enzyme [103] The maximum titres of extracellularlaccase in cultures of Lentinula edodes and Grifola frondosawere grown in liquid medium with 10 gL glucose [104 105]Glucose at 5 gL in the liquid medium supported laccaseproduction by Trametes gallica [68] Maximum laccase pro-duction was obtained using response surface methodologywith glucose (1521 gL) as the carbon source for Pleurotusflorida NCIM 1243 [106]

Among several carbon sources tested malt extract turnedout to be the best carbon source in the medium for pro-nounced laccase production by Phlebia floridensis P brevis-pora P radiata and P fascicularia [107] DrsquoSouza-Ticlo et al[108] screened different carbon sources for maximum laccaseproduction byBotryosphaeria spThey have screened glucosefructose galactose galacturonic acid xylose lactose sucrosemannitol pectin and inulin and found increased laccaseproduction with most carbon sources studied except inulinand galacturonic acid Revankar and Lele [109] obtainedhighest laccase activities with Trametes versicolor MTCC 138using different carbon sources namely glucose fructosesucrose lactose starch and glycerol They observed a 3-fold increase of laccase production when glucose was usedinstead of fructose and starch further improved laccaseproduction by 12 The carbon source mannitol increasedlaccase enzymatic activity to 11562 in Ganoderma lucidumstrain 7071-9 in Pichia pastoris at a concentration of 1mM buthad no effect at 01mM [110]

44 Influence of Nitrogen Sources on Laccase ProductionLaccases of white-rot fungi are mainly activated during thesecondary metabolic phase of the fungus and are oftentriggered by nitrogen depletion [111] but it was also foundthat in some strains nitrogen concentrations had no effect onlaccase activity [112] These contradictory observations wereascribed to differences between the strains of Phanerochaetechrysosporium and Lentinus edodes [86] Buswell et al [86]found that laccases were produced at high nitrogen concen-trations although it is generally accepted that a high carbonto nitrogen ratio is required for laccase production Laccasewas also produced earlier when the fungus was cultivatedin a substrate with a high nitrogen concentration and thesechanges did not reflect differences in biomass Heinzkill et al[83] also reported a higher yield of laccase using nitrogenrich media rather than the nitrogen limited media usuallyemployed for induction of oxidoreductase In another studyby [113] a rise in nitrogen concentration (from025 to 20 gL)enhanced laccase synthesis yield Higher nitrogen levels areoften required in order to enhance laccase production [114]but with certain fungi nitrogen-limited culture conditions

Enzyme Research 5

simulate the formation of laccase enzyme [111 115] Theystated that the culture parameter with the most deleteriouseffect on extracellular enzyme activity was of high levelnitrogen concentration

The optimum nitrogen concentration for obtainingthe highest laccase activity from Pycnoporus sanguineus(820mUmLminus1) is provided by a sucrose-asparagine mediumcontaining 5 times as much asparagine as Kirkrsquos mediumin fact such a medium provided a 25 times higher laccaseactivity than reference medium These conditions yieldedmaximum laccase activity [116] Laccase was best producedat the concentration of 100mgNH

4Cl and 50mgmalt extract

with gross yield of 0725UmL [117]Thenitrogen source thatimproved laccase synthesis to the greatest extent was peptone(18-fold increase) [95] Revankar and Lele [109] obtainedhighest laccase activities by Trametes versicolor MTCC 138using a complex nitrogen source (yeast extract) Leatham andKent Kirk [111] screened different nitrogen sources namelyKNO3 glutamic acid glycine beef extract and corn steep

liquor and found that glutamic acid with low concentrationyielded higher amounts of laccase

45 Influence of Aromatic Compounds on Laccase ProductionLow molecular weight aromatic compounds have shownsignificant influence on the growth and activity of lignocel-lulolytic microorganisms [118] Several compounds with amethylated p-phenolic group are the products of ferulic andsyringic acid metabolism in Phanerochaete chrysosporium[119] Aromatic compounds which are structurally relatedto lignin such as xylidine ferulic acid and veratric acidare routinely added to fungal cultures to increase laccaseproduction [105 120] Xylidine is known to increase laccasetranscription in Trametes villosa [121] Trametes versicolor[122] and P sajor-caju [123] It has been reported that one ofthe possible functions for fungal laccase is the polymerizationof toxic aromatic compounds formed during the degradationof lignin [8] A dark precipitate was observed in xylidine-induced cultures of T versicolor and has been suggested thatit may represent a laccase polymerized form of aromaticcompounds [122] Earlier studies on white-rot fungi haveshown that methylation of lignin-related aromatics inhibitsfungal growth only at higher concentrations (5 and 10mM)with stimulation occurring at 1mM concentration [124]Veratryl (3 4-dimethoxybenzyl) alcohol is an aromatic com-pound known to play an important role in the synthesis anddegradation of lignin

The addition of veratryl alcohol to cultivation mediaof many white-rot fungi has resulted in an increase inlaccase production [125] Some of these compounds affect themetabolismor growth rate [126]while others such as ethanolindirectly trigger laccase production [127] Many of thesecompounds resemble lignin molecules or other phenolicchemicals [105]There aremany reports describing the differ-ent effects of aromatic compounds on laccase activityHighestlaccase activity was observed in Botryosphaeria rhodinawhenveratryl alcohol was added to the nutrient medium at thebeginning of fermentation [128] R lignosus shows maxi-mum laccase activity with compound with phenylhydrazine[128] In a study by Elisashvili and Kachlishvili 2 4 6-tri-

nitrotoluene (TNT) supplemented medium at appropriateconcentration significantly accelerated Cerrena unicolor lac-case production and 4-fold increased laccase specific activity[129] Xylidine is known to increase laccase transcription inTrametes villosa [120] and in Trametes versicolor [121 130]The addition of veratryl alcohol to cultivation media of manywhite-rot fungi has resulted in an increase in laccase pro-duction [124 130] The aromatic compound hydroquinoneincreased 3-fold T versicolor laccase activity while decreas-ing 2- and 8-fold yields of MnP and endoglucanase [131]Hadibarata et al [132] have proved the importance of extra-cellular laccase of Armillaria sp F022 in the transformationof anthracene into anthraquinone benzoic acid and otherproducts such as 2-hydroxy-3-naphthoic acid and coumarin

46 Influence of Amino Acids on Laccase Production Lac-case production by white-rot fungi is strongly affected bythe presence of amino acids in the media [68] Variousamino acids and their analogues have shown stimulatory aswell as inhibitory effects on laccase production by Cyathusbulleri [133] According to this study DL-methionine DL-tryptophan glycine and DL-valine stimulated laccase pro-duction while L-cysteine monohydrochloride completelyinhibited the enzyme production Dong et al [68] usedamino acidmixture that contained the following amino acidsL-arginine L-histidine L-valine L-threonine L-isoleucineL-tyrosine L-methionine L-serine L-asparagine L-lysineL-aspartic acid L-tryptophan and L-cysteine at 1 (wv)concentration This amino acid mixture favoured the laccaseproduction by Trametes gallica It is possible that amino acidsact as inducer for laccase production bymanywhite-rot fungi[68 133] Sun et al [110] reported that all the six aminoacids (alanine histidine glycine arginine aspartate andphenylalanine) at 1mM concentration increase the catalyticability of the laccase enzyme from Ganoderma lucidumstrain 7071-9 when expressed in Pichia pastoris Amino acidtryptophan also induces laccase production in Crinipellis spRCK-1 [134]

47 Influence of Copper on Laccase Production Copper is anindispensable micronutrient for most living organisms andcopper requirements by microorganisms are usually satisfiedby low concentrations of the metal [105] In its free formcupric ion at higher concentration is extremely toxic tomicrobial cells The binding and uptake of copper in fungiusually comprise two phases metabolism-independent sur-face binding followed by an energy-dependent metal influx[135] The stimulatory effect of copper on laccase synthesiswas also effective for several other basidiomycetes and hencecould be used as a simple method to improve the productionof this enzyme [136] Using northern blot analysis it wasdetermined that increased production of laccase activitywould be obtained in the copper supplemented cultures ofPleurotus ostreatus [65]

Copper has been reported to be a strong laccase inducerin several species for example Neurospora crassa [137]Trametes versicolor [122] Phanerochaete chrysosporium [138]Panus osteratus [65] Pleurotus sajor-caju [123] Trametes

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

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[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

2 Enzyme Research

tree Rhus vernicifera [8] In 1896 laccase was demonstratedto be a fungal enzyme for the first time by both Bertrand andLaborde [9] Laccases of fungi attract considerable attentiondue to their possible involvement in the transformation of awide variety of phenolic compounds including the polymericlignin and humic substances [10] Most lignolytic fungalspecies produce constitutively at least one laccase isoenzymeand laccases are also dominant among lignolytic enzymes inthe soil environment In addition laccase-mediated deligni-fication allows increasing the nutritional value of agroindus-trial byproducts for animal feed or soil fertilizer [11]

The fact that they only require molecular oxygen forcatalysis makes them suitable for biotechnological applica-tions for the transformation or immobilization of xenobioticcompounds [12] The major role of laccases in lignin andphenolic compound degradation has been evaluated in alarge number of biotechnological applications such as dyedegradation bioremediation of some toxic chemical wastes(eg chlorinated aromatic compounds polycyclic aromatichydrocarbons nitroaromatics and pesticides) and biosensordevelopments [11ndash13] Commercially laccases have been usedto delignify wood tissues produce ethanol and distinguishbetween morphine and codeine Research in recent yearshas been intense much of it elicited by the wide variety oflaccases their utility and their very interesting propertiesThe current status of knowledge with regard to fungal laccaseand their applications to protect environment is reviewed

2 Distribution and PhysiologicalFunctions of Laccases

Laccases are common enzymes in nature and are foundwidely in plants and fungi as well as in some bacteria andinsects [14]The physiological functions of these biocatalystswhich can be secreted or intracellular are different in thevarious organisms but they all catalyse polymerization ordepolymerization processes [15] As mentioned earlier thefirst laccase was reported in 1883 from Rhus vernicifera theJapanese lacquer tree from which the designation laccasewas derived and the enzyme was characterized as a metalcontaining oxidase [16] This makes it one of the earliestenzymes ever described Laccases have subsequently beendiscovered from other numerous plants [17] but the detectionand purification of plant laccases are often difficult becausecrude plant extracts contain a large number of oxidativeenzymes with broad substrate specificities [17] which isprobably the reason why detailed information about thebiochemical properties of plant laccase is limited HoweverRhus vernicifera laccase is an exception and has been exten-sively studied especially with regard to its spectroscopicproperties [18] R vernicifera laccase has also widely beenused in investigations of the general reaction mechanism oflaccases [19 20] Plant laccases are found in the xylem wherethey presumably oxidize monolignols in the early stages oflignification [21] and also participate in the radical-basedmechanisms of lignin polymer formation [22] In additionlaccases have been shown to be involved in the first steps ofhealing in wounded leaves [23] However the occurrence of

laccases in higher plants appears to be far more limited thanin fungi [24 25]

Only a few bacterial laccases have been described hith-ertoThe first bacterial laccase was detected in the plant root-associated bacterium ldquoAzospirillum lipoferumrdquo [26] whereit was shown to be involved in melanin formation [27]An atypical laccase containing six putative copper-bindingsites was discovered from Marinomonas mediterranea butno functional role has been assigned to this enzyme [28]Bacillus subtilis produces a thermostable CotA laccase whichparticipates in pigment production in the endospore coat[29] Laccases have also been found from Streptomyces cya-neus [30] and Streptomyces lavendulae [31] Although thereare also some other reports about laccase activity in bacteriait does not seem probable that laccases are common enzymesfrom certain prokaryotic groups [32] Bacterial laccase-likeproteins are intracellular or periplasmic protein [10] Laccasesproducing bacteria from different environmental sourceswith their possible physiological functions of laccase aregiven below B licheniformis is a novel melanogenic soilbacterium isolated from soil which protects strain from UVlight and the oxidants [33] It is involved in dimerization ofphenolic acids [34] Bacillus endospores producing laccasewere isolated from soil and the enzyme involved in phenoldegradation [5 35]

Laccase activity has been demonstrated in many fun-gal species belonging to ascomycetes and basidiomycetesand the enzyme has already been purified from manyspecies There are many records of laccase production byascomycetes Phytopathogenic ascomycetes like Melanocar-pus albomyces [36]Cerrena unicolor [37]Magnaporthe grisea[38] Trametes versicolor [14] Trichoderma reesei [39] andXylaria polymorpha [40]are examples for laccase productionand the enzyme was purified Besides in plant pathogenicspecies laccase production was also reported for some soilascomycete species from the genera Aspergillus Curvulariaand Penicillium [41] as well as some fresh water ascomycetes[42] Yeasts are a physiologically specific group of bothascomycetes and basidiomycetes Until now laccase wasonly purified from the human yeast pathogen Cryptococcus(Filobasidiella) neoformans This yeast produces true laccasecapable of oxidation of phenols and aminophenols andunable to oxidize tyrosine [43] The enzyme is tightly boundto the cell wall and contributes to the resistance to fungicides[44] Among physiological groups of fungi laccases are typ-ical of the wood-rotting basidiomycetes which cause whiterot and a related group of litter-decomposing saprotrophicfungi that is the species causing lignin degradation Almostall species of white-rot fungi were reported to produce laccasein varying degrees and the enzyme has been purified frommany species [45]

The majority of laccases characterized so far have beenderived from white-rot fungi which are efficient lignin deg-raders [46] Many fungi contain several laccase-encodinggenes but their biological roles are mostly not well under-stood [47] Agaricus bisporus [48] Botrytis cinerea [49]Coprinus cinereus [50] Phlebia radiata [51] Pleurotus ostrea-tus [52] and Trametes versicolor [53] were some examplesof basidiomycetes that produce laccases In addition to

Enzyme Research 3

plants bacteria and fungi laccases or laccase-like activitieshave been found in some insects where they have beensuggested to be active in cuticle sclerotization [54] Recentlylaccases have been represented as candidates for ligninmodification enzymes (ldquolignasesrdquo) in termites Predominantlaccase activities against DMP and ABTS were detected inthe fungus combs and fungi isolated from the nests of threegenera of fungus-growing termites that is MacrotermesOdontotermes andMicrotermes [55ndash57]

3 Screening of Fungal Species

Screening of laccase producing fungal species and theirvariants is important for selecting suitable laccase producingorganisms For this reason one usually relies on the use ofinexpensive rapid and sensitive testingmethodsThe screen-ing strategy must aim to identify fungal strains and enzymesthat will work under industrial conditions [58] Discoveryof novel laccases with different substrate specificities andimproved stabilities is important for industrial applicationsFungi that produce laccase have been screened for eitheron solid media containing coloured indicator compoundsthat facilitate the visual detection of laccase production[59] or with liquid cultivations monitored with enzymeactivity measurements [60] The use of coloured indicatorsis generally simpler as no sample handling and measurementare required As laccases oxidize various types of substratesseveral different compounds have been used as indicators forlaccase production

The traditional screening reagents tannic acid and gallicacid [61] have nowadays mostly been replaced with synthe-tic phenolic reagents such as guaiacol and syringaldazine[59 62] or with the polymeric dyes Remazol Brilliant BlueR (RBRR) and Poly R-478 [63] RBRR and Poly R-478are decolourized by lignin degrading fungi [64] and theproduction of laccase is observed as a colourless halo aroundmicrobial growth With guaiacol a positive reaction is indi-cated by the formation of a reddish brown halo [59] whilewith the tannic acid and gallic acid the positive reaction is adark-brown coloured zone [61] Kiiskinen et al [46] screenednovel laccase producing fungi by a plate method based onpolymeric dye compounds guaiacol and tannic acid

4 Cultural and NutritionalConditions for Laccase Production

Culture conditions and medium composition play a majorrole in enzyme expression Laccase production by fungi isstrongly affected by many fermentation parameters such astime of cultivation stationary or submerged cultures organicor inorganic compound concentrations inducer concentra-tion [65] aeration [66] and degradation or activation byprotease [67] Laccases are generally produced during thesecondary metabolism of white-rot fungi growing on naturalsubstrate or in submerged culture [2] Physiological demandsvary among white-rot fungi and considerable research hasbeen done on the influence of agitation pH temperaturecarbon nitrogen sources andmicroelements and their levels

Dong et al [68] compared laccase production byTrametesgallica on twelve media under static or shaking conditionsThey concluded that twelve culture media in addition tostatic and shaking conditions show great influence onamount and pattern of laccase isoenzymes from Trametesgallica Gayazov and Rodakiewicz-Nowak [69] reportedfaster laccase production under semicontinuous cultivationwith high aeration and culture mixing compared to staticconditionsWhenusing conical flasks for cultivation it shouldbe baffled to ensure a high oxygen transfer [70] Simi-larly Piscitelli et al [71] described the influence of variousphysiological factors on laccase formation in a number ofwhite-rot fungi Refined media are necessary for obtaininglarge amount of laccases that may be used in biochemicalanalysis and industrial application Extracellular laccases ofwhite-rot fungi exist in isozymes that may be inducible orconstitutive Ganoderma lucidum produced more than threelaccase isozymes in liquid culture [72] Pleurotus pulmonariusproduced three laccase isozymes among which the lcc1 andlcc2 isoforms were produced in noninduced cultures whilelcc3 was found only in induced-culture filtrates [73] At leastseven laccase isozymes were found in the basidiomyceteCECT 20197 [74]Three constitutive and four induced laccaseisozymes were found in Marasmius querocophilus strain17 [75] At least nine constitutive laccase isozymes weredescribed for Pleurotus sp [76] The pattern of isozymes hasbeen successfully applied in the identification of a numberof different microorganisms particularly fungi such as ecto-mycorrhiza [77] deuteromycetes [78] and basidiomycetes[79 80]

A common technique for comparison of isozyme patternsfrom different sources is the use of zymograms [81] Praveenet al [82] found that the production of high titres of thelaccase enzyme was not dependent on high biomass yieldsBut laccase production was found to be highly related to theconditions of cultivation of the fungus [82 83] and mediasupporting high biomass did not necessarily support highlaccase yields [84] The synthesis and activity of the laccasewere controlled during growth and can play an importantrole in pigment and fruiting body formation [8 85] Buswellet al [86] reported that the production of laccase wasstrongly affected by the nature and amounts of nutrientsespecially nitrogen and trace elements in the growthmediumLaccases were generally produced in low concentrations bylaccase producing fungi [87] but higher concentrations wereobtainable with the addition of various supplements tomedia[71] Laccase production by Phanerochaete chrysosporiumwas not detected in low or high nitrogen medium withglucose as the carbon source but was produced when theorganism was grown on low or high nitrogen medium withcellulose as the carbon source [88] whereas in the white-rot fungus Ganoderma lucidum higher levels of laccaseswere produced in high nitrogen medium with glucose asthe carbon source [89] Ligninolytic systems of white-rotfungi were mainly activated during the secondary metabolicphase and were often triggered by nitrogen concentration[86] or when carbon or sulfur became limited [83] Theaddition of xenobiotic compounds such as xylidine lignin

4 Enzyme Research

and veratryl alcohol was known to increase and induce lac-case activity [84] Towards maximization of laccase secretionwith culture additives Sinegani et al [90] studied laccaseproduction by Aspergillus terreus Armillaria sp Polyporussp and Phanerochaete chrysosporium in liquid culture mediatreated with N-ethyl aniline NN-dimethyl aniline and para-bromoaniline as a laccase inducer

Optimization of the production medium plays a majorrole in higher laccase production The Taguchi approachof OA DOE constitutes a simple methodology that selectsthe best conditions producing consistent performance Thisapproach led to an increase in laccase yield to 820ULfrom 485UL The increased production of laccase wasalso confirmed by the dye decolorization experiment whichshowed an increased decolorization of reactive blue 221 from45 to 846 in the same unit volume [91]

41 Influence of pH on Laccase Production ThepHof the cul-ture medium is critical and plays a significant role in thegrowth and laccase production of the organism There isnot much information available on the influence of pH onlaccase production but when fungi are grown in a mediumwith pH 50 laccase will be produced in excess [8] Mostreports indicated initial pH levels set between pH 4 and6 prior to inoculation but the levels were not controlledduringmost cultivations [87 92]The optimumpH of laccaseproduction as reported in many fungi falls between 50and 60 [14 93 94] Maximum titres of laccase and biomasswere observed in the medium adjusted to pH 60 by Fomessclerodermeus white-rot basidiomycetes The optimal rangefor the laccase isoforms secreted by Trametes pubescensfungal strain has been reported between pH 30 and 45potentially indicating that laccase may be produced andfunction optimally under conditions that are not favourableto growth [95] Laccases from fungi have been found in wideapplications ranging from the pharmaceutical sector to thepulp and paper industry but eukaryotic laccases generallyprefer low pH for better functioning In contrast bacteriallaccases can act and are more stable at wider pH range[96 97] With the advantage of immense environmentaladaptability and biochemical versatility prokaryotes deserveto be studied for their possible applications in industry as wellas in medical science [5]

42 Influence of Temperature on Laccase Production Temper-ature like any other physical parameters plays a vital rolein growth and laccase production of the organism It hasbeen found that the optimal temperature for fruiting bodyformation and laccase production is 25∘C in the presence oflight but 30∘C for laccase production when the cultures areincubated in the dark [8] In general the fungi were cultivatedat temperatures between 25∘C and 30∘C for optimal laccaseproduction [14]When cultivated at temperatures higher than30∘C the activity of laccase was reduced [98] The wood-decaying basidiomycete Steccherinum ochraceum isolate 1833was reported to produce three highly thermostable laccaseisoforms with maximum activities in the region 75ndash80∘C[99 100] Therefore it is proved that optimum production oflaccase can differ greatly from one strain to another

43 Influence of Carbon on Laccase Production Carbon is apart of all living organisms Breakdown of carbon sourcesliberates energy which is utilized by the organism for growthand development The most readily usable carbon source bywhite-rot fungi is glucose [101] Collins and Dobson [102]reported that glucose at 10 gL enhanced the growth and lac-case production by Coriolus versicolor In Trametes versicolorglucose at higher concentration (20 gL) favoured laccaseproduction [14] In Ganoderma lucidum glucose at 20 gLincreased the mycelial growth but at 10 gL favoured expres-sion of enzyme [103] The maximum titres of extracellularlaccase in cultures of Lentinula edodes and Grifola frondosawere grown in liquid medium with 10 gL glucose [104 105]Glucose at 5 gL in the liquid medium supported laccaseproduction by Trametes gallica [68] Maximum laccase pro-duction was obtained using response surface methodologywith glucose (1521 gL) as the carbon source for Pleurotusflorida NCIM 1243 [106]

Among several carbon sources tested malt extract turnedout to be the best carbon source in the medium for pro-nounced laccase production by Phlebia floridensis P brevis-pora P radiata and P fascicularia [107] DrsquoSouza-Ticlo et al[108] screened different carbon sources for maximum laccaseproduction byBotryosphaeria spThey have screened glucosefructose galactose galacturonic acid xylose lactose sucrosemannitol pectin and inulin and found increased laccaseproduction with most carbon sources studied except inulinand galacturonic acid Revankar and Lele [109] obtainedhighest laccase activities with Trametes versicolor MTCC 138using different carbon sources namely glucose fructosesucrose lactose starch and glycerol They observed a 3-fold increase of laccase production when glucose was usedinstead of fructose and starch further improved laccaseproduction by 12 The carbon source mannitol increasedlaccase enzymatic activity to 11562 in Ganoderma lucidumstrain 7071-9 in Pichia pastoris at a concentration of 1mM buthad no effect at 01mM [110]

44 Influence of Nitrogen Sources on Laccase ProductionLaccases of white-rot fungi are mainly activated during thesecondary metabolic phase of the fungus and are oftentriggered by nitrogen depletion [111] but it was also foundthat in some strains nitrogen concentrations had no effect onlaccase activity [112] These contradictory observations wereascribed to differences between the strains of Phanerochaetechrysosporium and Lentinus edodes [86] Buswell et al [86]found that laccases were produced at high nitrogen concen-trations although it is generally accepted that a high carbonto nitrogen ratio is required for laccase production Laccasewas also produced earlier when the fungus was cultivatedin a substrate with a high nitrogen concentration and thesechanges did not reflect differences in biomass Heinzkill et al[83] also reported a higher yield of laccase using nitrogenrich media rather than the nitrogen limited media usuallyemployed for induction of oxidoreductase In another studyby [113] a rise in nitrogen concentration (from025 to 20 gL)enhanced laccase synthesis yield Higher nitrogen levels areoften required in order to enhance laccase production [114]but with certain fungi nitrogen-limited culture conditions

Enzyme Research 5

simulate the formation of laccase enzyme [111 115] Theystated that the culture parameter with the most deleteriouseffect on extracellular enzyme activity was of high levelnitrogen concentration

The optimum nitrogen concentration for obtainingthe highest laccase activity from Pycnoporus sanguineus(820mUmLminus1) is provided by a sucrose-asparagine mediumcontaining 5 times as much asparagine as Kirkrsquos mediumin fact such a medium provided a 25 times higher laccaseactivity than reference medium These conditions yieldedmaximum laccase activity [116] Laccase was best producedat the concentration of 100mgNH

4Cl and 50mgmalt extract

with gross yield of 0725UmL [117]Thenitrogen source thatimproved laccase synthesis to the greatest extent was peptone(18-fold increase) [95] Revankar and Lele [109] obtainedhighest laccase activities by Trametes versicolor MTCC 138using a complex nitrogen source (yeast extract) Leatham andKent Kirk [111] screened different nitrogen sources namelyKNO3 glutamic acid glycine beef extract and corn steep

liquor and found that glutamic acid with low concentrationyielded higher amounts of laccase

45 Influence of Aromatic Compounds on Laccase ProductionLow molecular weight aromatic compounds have shownsignificant influence on the growth and activity of lignocel-lulolytic microorganisms [118] Several compounds with amethylated p-phenolic group are the products of ferulic andsyringic acid metabolism in Phanerochaete chrysosporium[119] Aromatic compounds which are structurally relatedto lignin such as xylidine ferulic acid and veratric acidare routinely added to fungal cultures to increase laccaseproduction [105 120] Xylidine is known to increase laccasetranscription in Trametes villosa [121] Trametes versicolor[122] and P sajor-caju [123] It has been reported that one ofthe possible functions for fungal laccase is the polymerizationof toxic aromatic compounds formed during the degradationof lignin [8] A dark precipitate was observed in xylidine-induced cultures of T versicolor and has been suggested thatit may represent a laccase polymerized form of aromaticcompounds [122] Earlier studies on white-rot fungi haveshown that methylation of lignin-related aromatics inhibitsfungal growth only at higher concentrations (5 and 10mM)with stimulation occurring at 1mM concentration [124]Veratryl (3 4-dimethoxybenzyl) alcohol is an aromatic com-pound known to play an important role in the synthesis anddegradation of lignin

The addition of veratryl alcohol to cultivation mediaof many white-rot fungi has resulted in an increase inlaccase production [125] Some of these compounds affect themetabolismor growth rate [126]while others such as ethanolindirectly trigger laccase production [127] Many of thesecompounds resemble lignin molecules or other phenolicchemicals [105]There aremany reports describing the differ-ent effects of aromatic compounds on laccase activityHighestlaccase activity was observed in Botryosphaeria rhodinawhenveratryl alcohol was added to the nutrient medium at thebeginning of fermentation [128] R lignosus shows maxi-mum laccase activity with compound with phenylhydrazine[128] In a study by Elisashvili and Kachlishvili 2 4 6-tri-

nitrotoluene (TNT) supplemented medium at appropriateconcentration significantly accelerated Cerrena unicolor lac-case production and 4-fold increased laccase specific activity[129] Xylidine is known to increase laccase transcription inTrametes villosa [120] and in Trametes versicolor [121 130]The addition of veratryl alcohol to cultivation media of manywhite-rot fungi has resulted in an increase in laccase pro-duction [124 130] The aromatic compound hydroquinoneincreased 3-fold T versicolor laccase activity while decreas-ing 2- and 8-fold yields of MnP and endoglucanase [131]Hadibarata et al [132] have proved the importance of extra-cellular laccase of Armillaria sp F022 in the transformationof anthracene into anthraquinone benzoic acid and otherproducts such as 2-hydroxy-3-naphthoic acid and coumarin

46 Influence of Amino Acids on Laccase Production Lac-case production by white-rot fungi is strongly affected bythe presence of amino acids in the media [68] Variousamino acids and their analogues have shown stimulatory aswell as inhibitory effects on laccase production by Cyathusbulleri [133] According to this study DL-methionine DL-tryptophan glycine and DL-valine stimulated laccase pro-duction while L-cysteine monohydrochloride completelyinhibited the enzyme production Dong et al [68] usedamino acidmixture that contained the following amino acidsL-arginine L-histidine L-valine L-threonine L-isoleucineL-tyrosine L-methionine L-serine L-asparagine L-lysineL-aspartic acid L-tryptophan and L-cysteine at 1 (wv)concentration This amino acid mixture favoured the laccaseproduction by Trametes gallica It is possible that amino acidsact as inducer for laccase production bymanywhite-rot fungi[68 133] Sun et al [110] reported that all the six aminoacids (alanine histidine glycine arginine aspartate andphenylalanine) at 1mM concentration increase the catalyticability of the laccase enzyme from Ganoderma lucidumstrain 7071-9 when expressed in Pichia pastoris Amino acidtryptophan also induces laccase production in Crinipellis spRCK-1 [134]

47 Influence of Copper on Laccase Production Copper is anindispensable micronutrient for most living organisms andcopper requirements by microorganisms are usually satisfiedby low concentrations of the metal [105] In its free formcupric ion at higher concentration is extremely toxic tomicrobial cells The binding and uptake of copper in fungiusually comprise two phases metabolism-independent sur-face binding followed by an energy-dependent metal influx[135] The stimulatory effect of copper on laccase synthesiswas also effective for several other basidiomycetes and hencecould be used as a simple method to improve the productionof this enzyme [136] Using northern blot analysis it wasdetermined that increased production of laccase activitywould be obtained in the copper supplemented cultures ofPleurotus ostreatus [65]

Copper has been reported to be a strong laccase inducerin several species for example Neurospora crassa [137]Trametes versicolor [122] Phanerochaete chrysosporium [138]Panus osteratus [65] Pleurotus sajor-caju [123] Trametes

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 3

plants bacteria and fungi laccases or laccase-like activitieshave been found in some insects where they have beensuggested to be active in cuticle sclerotization [54] Recentlylaccases have been represented as candidates for ligninmodification enzymes (ldquolignasesrdquo) in termites Predominantlaccase activities against DMP and ABTS were detected inthe fungus combs and fungi isolated from the nests of threegenera of fungus-growing termites that is MacrotermesOdontotermes andMicrotermes [55ndash57]

3 Screening of Fungal Species

Screening of laccase producing fungal species and theirvariants is important for selecting suitable laccase producingorganisms For this reason one usually relies on the use ofinexpensive rapid and sensitive testingmethodsThe screen-ing strategy must aim to identify fungal strains and enzymesthat will work under industrial conditions [58] Discoveryof novel laccases with different substrate specificities andimproved stabilities is important for industrial applicationsFungi that produce laccase have been screened for eitheron solid media containing coloured indicator compoundsthat facilitate the visual detection of laccase production[59] or with liquid cultivations monitored with enzymeactivity measurements [60] The use of coloured indicatorsis generally simpler as no sample handling and measurementare required As laccases oxidize various types of substratesseveral different compounds have been used as indicators forlaccase production

The traditional screening reagents tannic acid and gallicacid [61] have nowadays mostly been replaced with synthe-tic phenolic reagents such as guaiacol and syringaldazine[59 62] or with the polymeric dyes Remazol Brilliant BlueR (RBRR) and Poly R-478 [63] RBRR and Poly R-478are decolourized by lignin degrading fungi [64] and theproduction of laccase is observed as a colourless halo aroundmicrobial growth With guaiacol a positive reaction is indi-cated by the formation of a reddish brown halo [59] whilewith the tannic acid and gallic acid the positive reaction is adark-brown coloured zone [61] Kiiskinen et al [46] screenednovel laccase producing fungi by a plate method based onpolymeric dye compounds guaiacol and tannic acid

4 Cultural and NutritionalConditions for Laccase Production

Culture conditions and medium composition play a majorrole in enzyme expression Laccase production by fungi isstrongly affected by many fermentation parameters such astime of cultivation stationary or submerged cultures organicor inorganic compound concentrations inducer concentra-tion [65] aeration [66] and degradation or activation byprotease [67] Laccases are generally produced during thesecondary metabolism of white-rot fungi growing on naturalsubstrate or in submerged culture [2] Physiological demandsvary among white-rot fungi and considerable research hasbeen done on the influence of agitation pH temperaturecarbon nitrogen sources andmicroelements and their levels

Dong et al [68] compared laccase production byTrametesgallica on twelve media under static or shaking conditionsThey concluded that twelve culture media in addition tostatic and shaking conditions show great influence onamount and pattern of laccase isoenzymes from Trametesgallica Gayazov and Rodakiewicz-Nowak [69] reportedfaster laccase production under semicontinuous cultivationwith high aeration and culture mixing compared to staticconditionsWhenusing conical flasks for cultivation it shouldbe baffled to ensure a high oxygen transfer [70] Simi-larly Piscitelli et al [71] described the influence of variousphysiological factors on laccase formation in a number ofwhite-rot fungi Refined media are necessary for obtaininglarge amount of laccases that may be used in biochemicalanalysis and industrial application Extracellular laccases ofwhite-rot fungi exist in isozymes that may be inducible orconstitutive Ganoderma lucidum produced more than threelaccase isozymes in liquid culture [72] Pleurotus pulmonariusproduced three laccase isozymes among which the lcc1 andlcc2 isoforms were produced in noninduced cultures whilelcc3 was found only in induced-culture filtrates [73] At leastseven laccase isozymes were found in the basidiomyceteCECT 20197 [74]Three constitutive and four induced laccaseisozymes were found in Marasmius querocophilus strain17 [75] At least nine constitutive laccase isozymes weredescribed for Pleurotus sp [76] The pattern of isozymes hasbeen successfully applied in the identification of a numberof different microorganisms particularly fungi such as ecto-mycorrhiza [77] deuteromycetes [78] and basidiomycetes[79 80]

A common technique for comparison of isozyme patternsfrom different sources is the use of zymograms [81] Praveenet al [82] found that the production of high titres of thelaccase enzyme was not dependent on high biomass yieldsBut laccase production was found to be highly related to theconditions of cultivation of the fungus [82 83] and mediasupporting high biomass did not necessarily support highlaccase yields [84] The synthesis and activity of the laccasewere controlled during growth and can play an importantrole in pigment and fruiting body formation [8 85] Buswellet al [86] reported that the production of laccase wasstrongly affected by the nature and amounts of nutrientsespecially nitrogen and trace elements in the growthmediumLaccases were generally produced in low concentrations bylaccase producing fungi [87] but higher concentrations wereobtainable with the addition of various supplements tomedia[71] Laccase production by Phanerochaete chrysosporiumwas not detected in low or high nitrogen medium withglucose as the carbon source but was produced when theorganism was grown on low or high nitrogen medium withcellulose as the carbon source [88] whereas in the white-rot fungus Ganoderma lucidum higher levels of laccaseswere produced in high nitrogen medium with glucose asthe carbon source [89] Ligninolytic systems of white-rotfungi were mainly activated during the secondary metabolicphase and were often triggered by nitrogen concentration[86] or when carbon or sulfur became limited [83] Theaddition of xenobiotic compounds such as xylidine lignin

4 Enzyme Research

and veratryl alcohol was known to increase and induce lac-case activity [84] Towards maximization of laccase secretionwith culture additives Sinegani et al [90] studied laccaseproduction by Aspergillus terreus Armillaria sp Polyporussp and Phanerochaete chrysosporium in liquid culture mediatreated with N-ethyl aniline NN-dimethyl aniline and para-bromoaniline as a laccase inducer

Optimization of the production medium plays a majorrole in higher laccase production The Taguchi approachof OA DOE constitutes a simple methodology that selectsthe best conditions producing consistent performance Thisapproach led to an increase in laccase yield to 820ULfrom 485UL The increased production of laccase wasalso confirmed by the dye decolorization experiment whichshowed an increased decolorization of reactive blue 221 from45 to 846 in the same unit volume [91]

41 Influence of pH on Laccase Production ThepHof the cul-ture medium is critical and plays a significant role in thegrowth and laccase production of the organism There isnot much information available on the influence of pH onlaccase production but when fungi are grown in a mediumwith pH 50 laccase will be produced in excess [8] Mostreports indicated initial pH levels set between pH 4 and6 prior to inoculation but the levels were not controlledduringmost cultivations [87 92]The optimumpH of laccaseproduction as reported in many fungi falls between 50and 60 [14 93 94] Maximum titres of laccase and biomasswere observed in the medium adjusted to pH 60 by Fomessclerodermeus white-rot basidiomycetes The optimal rangefor the laccase isoforms secreted by Trametes pubescensfungal strain has been reported between pH 30 and 45potentially indicating that laccase may be produced andfunction optimally under conditions that are not favourableto growth [95] Laccases from fungi have been found in wideapplications ranging from the pharmaceutical sector to thepulp and paper industry but eukaryotic laccases generallyprefer low pH for better functioning In contrast bacteriallaccases can act and are more stable at wider pH range[96 97] With the advantage of immense environmentaladaptability and biochemical versatility prokaryotes deserveto be studied for their possible applications in industry as wellas in medical science [5]

42 Influence of Temperature on Laccase Production Temper-ature like any other physical parameters plays a vital rolein growth and laccase production of the organism It hasbeen found that the optimal temperature for fruiting bodyformation and laccase production is 25∘C in the presence oflight but 30∘C for laccase production when the cultures areincubated in the dark [8] In general the fungi were cultivatedat temperatures between 25∘C and 30∘C for optimal laccaseproduction [14]When cultivated at temperatures higher than30∘C the activity of laccase was reduced [98] The wood-decaying basidiomycete Steccherinum ochraceum isolate 1833was reported to produce three highly thermostable laccaseisoforms with maximum activities in the region 75ndash80∘C[99 100] Therefore it is proved that optimum production oflaccase can differ greatly from one strain to another

43 Influence of Carbon on Laccase Production Carbon is apart of all living organisms Breakdown of carbon sourcesliberates energy which is utilized by the organism for growthand development The most readily usable carbon source bywhite-rot fungi is glucose [101] Collins and Dobson [102]reported that glucose at 10 gL enhanced the growth and lac-case production by Coriolus versicolor In Trametes versicolorglucose at higher concentration (20 gL) favoured laccaseproduction [14] In Ganoderma lucidum glucose at 20 gLincreased the mycelial growth but at 10 gL favoured expres-sion of enzyme [103] The maximum titres of extracellularlaccase in cultures of Lentinula edodes and Grifola frondosawere grown in liquid medium with 10 gL glucose [104 105]Glucose at 5 gL in the liquid medium supported laccaseproduction by Trametes gallica [68] Maximum laccase pro-duction was obtained using response surface methodologywith glucose (1521 gL) as the carbon source for Pleurotusflorida NCIM 1243 [106]

Among several carbon sources tested malt extract turnedout to be the best carbon source in the medium for pro-nounced laccase production by Phlebia floridensis P brevis-pora P radiata and P fascicularia [107] DrsquoSouza-Ticlo et al[108] screened different carbon sources for maximum laccaseproduction byBotryosphaeria spThey have screened glucosefructose galactose galacturonic acid xylose lactose sucrosemannitol pectin and inulin and found increased laccaseproduction with most carbon sources studied except inulinand galacturonic acid Revankar and Lele [109] obtainedhighest laccase activities with Trametes versicolor MTCC 138using different carbon sources namely glucose fructosesucrose lactose starch and glycerol They observed a 3-fold increase of laccase production when glucose was usedinstead of fructose and starch further improved laccaseproduction by 12 The carbon source mannitol increasedlaccase enzymatic activity to 11562 in Ganoderma lucidumstrain 7071-9 in Pichia pastoris at a concentration of 1mM buthad no effect at 01mM [110]

44 Influence of Nitrogen Sources on Laccase ProductionLaccases of white-rot fungi are mainly activated during thesecondary metabolic phase of the fungus and are oftentriggered by nitrogen depletion [111] but it was also foundthat in some strains nitrogen concentrations had no effect onlaccase activity [112] These contradictory observations wereascribed to differences between the strains of Phanerochaetechrysosporium and Lentinus edodes [86] Buswell et al [86]found that laccases were produced at high nitrogen concen-trations although it is generally accepted that a high carbonto nitrogen ratio is required for laccase production Laccasewas also produced earlier when the fungus was cultivatedin a substrate with a high nitrogen concentration and thesechanges did not reflect differences in biomass Heinzkill et al[83] also reported a higher yield of laccase using nitrogenrich media rather than the nitrogen limited media usuallyemployed for induction of oxidoreductase In another studyby [113] a rise in nitrogen concentration (from025 to 20 gL)enhanced laccase synthesis yield Higher nitrogen levels areoften required in order to enhance laccase production [114]but with certain fungi nitrogen-limited culture conditions

Enzyme Research 5

simulate the formation of laccase enzyme [111 115] Theystated that the culture parameter with the most deleteriouseffect on extracellular enzyme activity was of high levelnitrogen concentration

The optimum nitrogen concentration for obtainingthe highest laccase activity from Pycnoporus sanguineus(820mUmLminus1) is provided by a sucrose-asparagine mediumcontaining 5 times as much asparagine as Kirkrsquos mediumin fact such a medium provided a 25 times higher laccaseactivity than reference medium These conditions yieldedmaximum laccase activity [116] Laccase was best producedat the concentration of 100mgNH

4Cl and 50mgmalt extract

with gross yield of 0725UmL [117]Thenitrogen source thatimproved laccase synthesis to the greatest extent was peptone(18-fold increase) [95] Revankar and Lele [109] obtainedhighest laccase activities by Trametes versicolor MTCC 138using a complex nitrogen source (yeast extract) Leatham andKent Kirk [111] screened different nitrogen sources namelyKNO3 glutamic acid glycine beef extract and corn steep

liquor and found that glutamic acid with low concentrationyielded higher amounts of laccase

45 Influence of Aromatic Compounds on Laccase ProductionLow molecular weight aromatic compounds have shownsignificant influence on the growth and activity of lignocel-lulolytic microorganisms [118] Several compounds with amethylated p-phenolic group are the products of ferulic andsyringic acid metabolism in Phanerochaete chrysosporium[119] Aromatic compounds which are structurally relatedto lignin such as xylidine ferulic acid and veratric acidare routinely added to fungal cultures to increase laccaseproduction [105 120] Xylidine is known to increase laccasetranscription in Trametes villosa [121] Trametes versicolor[122] and P sajor-caju [123] It has been reported that one ofthe possible functions for fungal laccase is the polymerizationof toxic aromatic compounds formed during the degradationof lignin [8] A dark precipitate was observed in xylidine-induced cultures of T versicolor and has been suggested thatit may represent a laccase polymerized form of aromaticcompounds [122] Earlier studies on white-rot fungi haveshown that methylation of lignin-related aromatics inhibitsfungal growth only at higher concentrations (5 and 10mM)with stimulation occurring at 1mM concentration [124]Veratryl (3 4-dimethoxybenzyl) alcohol is an aromatic com-pound known to play an important role in the synthesis anddegradation of lignin

The addition of veratryl alcohol to cultivation mediaof many white-rot fungi has resulted in an increase inlaccase production [125] Some of these compounds affect themetabolismor growth rate [126]while others such as ethanolindirectly trigger laccase production [127] Many of thesecompounds resemble lignin molecules or other phenolicchemicals [105]There aremany reports describing the differ-ent effects of aromatic compounds on laccase activityHighestlaccase activity was observed in Botryosphaeria rhodinawhenveratryl alcohol was added to the nutrient medium at thebeginning of fermentation [128] R lignosus shows maxi-mum laccase activity with compound with phenylhydrazine[128] In a study by Elisashvili and Kachlishvili 2 4 6-tri-

nitrotoluene (TNT) supplemented medium at appropriateconcentration significantly accelerated Cerrena unicolor lac-case production and 4-fold increased laccase specific activity[129] Xylidine is known to increase laccase transcription inTrametes villosa [120] and in Trametes versicolor [121 130]The addition of veratryl alcohol to cultivation media of manywhite-rot fungi has resulted in an increase in laccase pro-duction [124 130] The aromatic compound hydroquinoneincreased 3-fold T versicolor laccase activity while decreas-ing 2- and 8-fold yields of MnP and endoglucanase [131]Hadibarata et al [132] have proved the importance of extra-cellular laccase of Armillaria sp F022 in the transformationof anthracene into anthraquinone benzoic acid and otherproducts such as 2-hydroxy-3-naphthoic acid and coumarin

46 Influence of Amino Acids on Laccase Production Lac-case production by white-rot fungi is strongly affected bythe presence of amino acids in the media [68] Variousamino acids and their analogues have shown stimulatory aswell as inhibitory effects on laccase production by Cyathusbulleri [133] According to this study DL-methionine DL-tryptophan glycine and DL-valine stimulated laccase pro-duction while L-cysteine monohydrochloride completelyinhibited the enzyme production Dong et al [68] usedamino acidmixture that contained the following amino acidsL-arginine L-histidine L-valine L-threonine L-isoleucineL-tyrosine L-methionine L-serine L-asparagine L-lysineL-aspartic acid L-tryptophan and L-cysteine at 1 (wv)concentration This amino acid mixture favoured the laccaseproduction by Trametes gallica It is possible that amino acidsact as inducer for laccase production bymanywhite-rot fungi[68 133] Sun et al [110] reported that all the six aminoacids (alanine histidine glycine arginine aspartate andphenylalanine) at 1mM concentration increase the catalyticability of the laccase enzyme from Ganoderma lucidumstrain 7071-9 when expressed in Pichia pastoris Amino acidtryptophan also induces laccase production in Crinipellis spRCK-1 [134]

47 Influence of Copper on Laccase Production Copper is anindispensable micronutrient for most living organisms andcopper requirements by microorganisms are usually satisfiedby low concentrations of the metal [105] In its free formcupric ion at higher concentration is extremely toxic tomicrobial cells The binding and uptake of copper in fungiusually comprise two phases metabolism-independent sur-face binding followed by an energy-dependent metal influx[135] The stimulatory effect of copper on laccase synthesiswas also effective for several other basidiomycetes and hencecould be used as a simple method to improve the productionof this enzyme [136] Using northern blot analysis it wasdetermined that increased production of laccase activitywould be obtained in the copper supplemented cultures ofPleurotus ostreatus [65]

Copper has been reported to be a strong laccase inducerin several species for example Neurospora crassa [137]Trametes versicolor [122] Phanerochaete chrysosporium [138]Panus osteratus [65] Pleurotus sajor-caju [123] Trametes

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

4 Enzyme Research

and veratryl alcohol was known to increase and induce lac-case activity [84] Towards maximization of laccase secretionwith culture additives Sinegani et al [90] studied laccaseproduction by Aspergillus terreus Armillaria sp Polyporussp and Phanerochaete chrysosporium in liquid culture mediatreated with N-ethyl aniline NN-dimethyl aniline and para-bromoaniline as a laccase inducer

Optimization of the production medium plays a majorrole in higher laccase production The Taguchi approachof OA DOE constitutes a simple methodology that selectsthe best conditions producing consistent performance Thisapproach led to an increase in laccase yield to 820ULfrom 485UL The increased production of laccase wasalso confirmed by the dye decolorization experiment whichshowed an increased decolorization of reactive blue 221 from45 to 846 in the same unit volume [91]

41 Influence of pH on Laccase Production ThepHof the cul-ture medium is critical and plays a significant role in thegrowth and laccase production of the organism There isnot much information available on the influence of pH onlaccase production but when fungi are grown in a mediumwith pH 50 laccase will be produced in excess [8] Mostreports indicated initial pH levels set between pH 4 and6 prior to inoculation but the levels were not controlledduringmost cultivations [87 92]The optimumpH of laccaseproduction as reported in many fungi falls between 50and 60 [14 93 94] Maximum titres of laccase and biomasswere observed in the medium adjusted to pH 60 by Fomessclerodermeus white-rot basidiomycetes The optimal rangefor the laccase isoforms secreted by Trametes pubescensfungal strain has been reported between pH 30 and 45potentially indicating that laccase may be produced andfunction optimally under conditions that are not favourableto growth [95] Laccases from fungi have been found in wideapplications ranging from the pharmaceutical sector to thepulp and paper industry but eukaryotic laccases generallyprefer low pH for better functioning In contrast bacteriallaccases can act and are more stable at wider pH range[96 97] With the advantage of immense environmentaladaptability and biochemical versatility prokaryotes deserveto be studied for their possible applications in industry as wellas in medical science [5]

42 Influence of Temperature on Laccase Production Temper-ature like any other physical parameters plays a vital rolein growth and laccase production of the organism It hasbeen found that the optimal temperature for fruiting bodyformation and laccase production is 25∘C in the presence oflight but 30∘C for laccase production when the cultures areincubated in the dark [8] In general the fungi were cultivatedat temperatures between 25∘C and 30∘C for optimal laccaseproduction [14]When cultivated at temperatures higher than30∘C the activity of laccase was reduced [98] The wood-decaying basidiomycete Steccherinum ochraceum isolate 1833was reported to produce three highly thermostable laccaseisoforms with maximum activities in the region 75ndash80∘C[99 100] Therefore it is proved that optimum production oflaccase can differ greatly from one strain to another

43 Influence of Carbon on Laccase Production Carbon is apart of all living organisms Breakdown of carbon sourcesliberates energy which is utilized by the organism for growthand development The most readily usable carbon source bywhite-rot fungi is glucose [101] Collins and Dobson [102]reported that glucose at 10 gL enhanced the growth and lac-case production by Coriolus versicolor In Trametes versicolorglucose at higher concentration (20 gL) favoured laccaseproduction [14] In Ganoderma lucidum glucose at 20 gLincreased the mycelial growth but at 10 gL favoured expres-sion of enzyme [103] The maximum titres of extracellularlaccase in cultures of Lentinula edodes and Grifola frondosawere grown in liquid medium with 10 gL glucose [104 105]Glucose at 5 gL in the liquid medium supported laccaseproduction by Trametes gallica [68] Maximum laccase pro-duction was obtained using response surface methodologywith glucose (1521 gL) as the carbon source for Pleurotusflorida NCIM 1243 [106]

Among several carbon sources tested malt extract turnedout to be the best carbon source in the medium for pro-nounced laccase production by Phlebia floridensis P brevis-pora P radiata and P fascicularia [107] DrsquoSouza-Ticlo et al[108] screened different carbon sources for maximum laccaseproduction byBotryosphaeria spThey have screened glucosefructose galactose galacturonic acid xylose lactose sucrosemannitol pectin and inulin and found increased laccaseproduction with most carbon sources studied except inulinand galacturonic acid Revankar and Lele [109] obtainedhighest laccase activities with Trametes versicolor MTCC 138using different carbon sources namely glucose fructosesucrose lactose starch and glycerol They observed a 3-fold increase of laccase production when glucose was usedinstead of fructose and starch further improved laccaseproduction by 12 The carbon source mannitol increasedlaccase enzymatic activity to 11562 in Ganoderma lucidumstrain 7071-9 in Pichia pastoris at a concentration of 1mM buthad no effect at 01mM [110]

44 Influence of Nitrogen Sources on Laccase ProductionLaccases of white-rot fungi are mainly activated during thesecondary metabolic phase of the fungus and are oftentriggered by nitrogen depletion [111] but it was also foundthat in some strains nitrogen concentrations had no effect onlaccase activity [112] These contradictory observations wereascribed to differences between the strains of Phanerochaetechrysosporium and Lentinus edodes [86] Buswell et al [86]found that laccases were produced at high nitrogen concen-trations although it is generally accepted that a high carbonto nitrogen ratio is required for laccase production Laccasewas also produced earlier when the fungus was cultivatedin a substrate with a high nitrogen concentration and thesechanges did not reflect differences in biomass Heinzkill et al[83] also reported a higher yield of laccase using nitrogenrich media rather than the nitrogen limited media usuallyemployed for induction of oxidoreductase In another studyby [113] a rise in nitrogen concentration (from025 to 20 gL)enhanced laccase synthesis yield Higher nitrogen levels areoften required in order to enhance laccase production [114]but with certain fungi nitrogen-limited culture conditions

Enzyme Research 5

simulate the formation of laccase enzyme [111 115] Theystated that the culture parameter with the most deleteriouseffect on extracellular enzyme activity was of high levelnitrogen concentration

The optimum nitrogen concentration for obtainingthe highest laccase activity from Pycnoporus sanguineus(820mUmLminus1) is provided by a sucrose-asparagine mediumcontaining 5 times as much asparagine as Kirkrsquos mediumin fact such a medium provided a 25 times higher laccaseactivity than reference medium These conditions yieldedmaximum laccase activity [116] Laccase was best producedat the concentration of 100mgNH

4Cl and 50mgmalt extract

with gross yield of 0725UmL [117]Thenitrogen source thatimproved laccase synthesis to the greatest extent was peptone(18-fold increase) [95] Revankar and Lele [109] obtainedhighest laccase activities by Trametes versicolor MTCC 138using a complex nitrogen source (yeast extract) Leatham andKent Kirk [111] screened different nitrogen sources namelyKNO3 glutamic acid glycine beef extract and corn steep

liquor and found that glutamic acid with low concentrationyielded higher amounts of laccase

45 Influence of Aromatic Compounds on Laccase ProductionLow molecular weight aromatic compounds have shownsignificant influence on the growth and activity of lignocel-lulolytic microorganisms [118] Several compounds with amethylated p-phenolic group are the products of ferulic andsyringic acid metabolism in Phanerochaete chrysosporium[119] Aromatic compounds which are structurally relatedto lignin such as xylidine ferulic acid and veratric acidare routinely added to fungal cultures to increase laccaseproduction [105 120] Xylidine is known to increase laccasetranscription in Trametes villosa [121] Trametes versicolor[122] and P sajor-caju [123] It has been reported that one ofthe possible functions for fungal laccase is the polymerizationof toxic aromatic compounds formed during the degradationof lignin [8] A dark precipitate was observed in xylidine-induced cultures of T versicolor and has been suggested thatit may represent a laccase polymerized form of aromaticcompounds [122] Earlier studies on white-rot fungi haveshown that methylation of lignin-related aromatics inhibitsfungal growth only at higher concentrations (5 and 10mM)with stimulation occurring at 1mM concentration [124]Veratryl (3 4-dimethoxybenzyl) alcohol is an aromatic com-pound known to play an important role in the synthesis anddegradation of lignin

The addition of veratryl alcohol to cultivation mediaof many white-rot fungi has resulted in an increase inlaccase production [125] Some of these compounds affect themetabolismor growth rate [126]while others such as ethanolindirectly trigger laccase production [127] Many of thesecompounds resemble lignin molecules or other phenolicchemicals [105]There aremany reports describing the differ-ent effects of aromatic compounds on laccase activityHighestlaccase activity was observed in Botryosphaeria rhodinawhenveratryl alcohol was added to the nutrient medium at thebeginning of fermentation [128] R lignosus shows maxi-mum laccase activity with compound with phenylhydrazine[128] In a study by Elisashvili and Kachlishvili 2 4 6-tri-

nitrotoluene (TNT) supplemented medium at appropriateconcentration significantly accelerated Cerrena unicolor lac-case production and 4-fold increased laccase specific activity[129] Xylidine is known to increase laccase transcription inTrametes villosa [120] and in Trametes versicolor [121 130]The addition of veratryl alcohol to cultivation media of manywhite-rot fungi has resulted in an increase in laccase pro-duction [124 130] The aromatic compound hydroquinoneincreased 3-fold T versicolor laccase activity while decreas-ing 2- and 8-fold yields of MnP and endoglucanase [131]Hadibarata et al [132] have proved the importance of extra-cellular laccase of Armillaria sp F022 in the transformationof anthracene into anthraquinone benzoic acid and otherproducts such as 2-hydroxy-3-naphthoic acid and coumarin

46 Influence of Amino Acids on Laccase Production Lac-case production by white-rot fungi is strongly affected bythe presence of amino acids in the media [68] Variousamino acids and their analogues have shown stimulatory aswell as inhibitory effects on laccase production by Cyathusbulleri [133] According to this study DL-methionine DL-tryptophan glycine and DL-valine stimulated laccase pro-duction while L-cysteine monohydrochloride completelyinhibited the enzyme production Dong et al [68] usedamino acidmixture that contained the following amino acidsL-arginine L-histidine L-valine L-threonine L-isoleucineL-tyrosine L-methionine L-serine L-asparagine L-lysineL-aspartic acid L-tryptophan and L-cysteine at 1 (wv)concentration This amino acid mixture favoured the laccaseproduction by Trametes gallica It is possible that amino acidsact as inducer for laccase production bymanywhite-rot fungi[68 133] Sun et al [110] reported that all the six aminoacids (alanine histidine glycine arginine aspartate andphenylalanine) at 1mM concentration increase the catalyticability of the laccase enzyme from Ganoderma lucidumstrain 7071-9 when expressed in Pichia pastoris Amino acidtryptophan also induces laccase production in Crinipellis spRCK-1 [134]

47 Influence of Copper on Laccase Production Copper is anindispensable micronutrient for most living organisms andcopper requirements by microorganisms are usually satisfiedby low concentrations of the metal [105] In its free formcupric ion at higher concentration is extremely toxic tomicrobial cells The binding and uptake of copper in fungiusually comprise two phases metabolism-independent sur-face binding followed by an energy-dependent metal influx[135] The stimulatory effect of copper on laccase synthesiswas also effective for several other basidiomycetes and hencecould be used as a simple method to improve the productionof this enzyme [136] Using northern blot analysis it wasdetermined that increased production of laccase activitywould be obtained in the copper supplemented cultures ofPleurotus ostreatus [65]

Copper has been reported to be a strong laccase inducerin several species for example Neurospora crassa [137]Trametes versicolor [122] Phanerochaete chrysosporium [138]Panus osteratus [65] Pleurotus sajor-caju [123] Trametes

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

Volume 2014

Zoology

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Signal TransductionJournal of

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Enzyme Research

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International Journal of

Microbiology

Enzyme Research 5

simulate the formation of laccase enzyme [111 115] Theystated that the culture parameter with the most deleteriouseffect on extracellular enzyme activity was of high levelnitrogen concentration

The optimum nitrogen concentration for obtainingthe highest laccase activity from Pycnoporus sanguineus(820mUmLminus1) is provided by a sucrose-asparagine mediumcontaining 5 times as much asparagine as Kirkrsquos mediumin fact such a medium provided a 25 times higher laccaseactivity than reference medium These conditions yieldedmaximum laccase activity [116] Laccase was best producedat the concentration of 100mgNH

4Cl and 50mgmalt extract

with gross yield of 0725UmL [117]Thenitrogen source thatimproved laccase synthesis to the greatest extent was peptone(18-fold increase) [95] Revankar and Lele [109] obtainedhighest laccase activities by Trametes versicolor MTCC 138using a complex nitrogen source (yeast extract) Leatham andKent Kirk [111] screened different nitrogen sources namelyKNO3 glutamic acid glycine beef extract and corn steep

liquor and found that glutamic acid with low concentrationyielded higher amounts of laccase

45 Influence of Aromatic Compounds on Laccase ProductionLow molecular weight aromatic compounds have shownsignificant influence on the growth and activity of lignocel-lulolytic microorganisms [118] Several compounds with amethylated p-phenolic group are the products of ferulic andsyringic acid metabolism in Phanerochaete chrysosporium[119] Aromatic compounds which are structurally relatedto lignin such as xylidine ferulic acid and veratric acidare routinely added to fungal cultures to increase laccaseproduction [105 120] Xylidine is known to increase laccasetranscription in Trametes villosa [121] Trametes versicolor[122] and P sajor-caju [123] It has been reported that one ofthe possible functions for fungal laccase is the polymerizationof toxic aromatic compounds formed during the degradationof lignin [8] A dark precipitate was observed in xylidine-induced cultures of T versicolor and has been suggested thatit may represent a laccase polymerized form of aromaticcompounds [122] Earlier studies on white-rot fungi haveshown that methylation of lignin-related aromatics inhibitsfungal growth only at higher concentrations (5 and 10mM)with stimulation occurring at 1mM concentration [124]Veratryl (3 4-dimethoxybenzyl) alcohol is an aromatic com-pound known to play an important role in the synthesis anddegradation of lignin

The addition of veratryl alcohol to cultivation mediaof many white-rot fungi has resulted in an increase inlaccase production [125] Some of these compounds affect themetabolismor growth rate [126]while others such as ethanolindirectly trigger laccase production [127] Many of thesecompounds resemble lignin molecules or other phenolicchemicals [105]There aremany reports describing the differ-ent effects of aromatic compounds on laccase activityHighestlaccase activity was observed in Botryosphaeria rhodinawhenveratryl alcohol was added to the nutrient medium at thebeginning of fermentation [128] R lignosus shows maxi-mum laccase activity with compound with phenylhydrazine[128] In a study by Elisashvili and Kachlishvili 2 4 6-tri-

nitrotoluene (TNT) supplemented medium at appropriateconcentration significantly accelerated Cerrena unicolor lac-case production and 4-fold increased laccase specific activity[129] Xylidine is known to increase laccase transcription inTrametes villosa [120] and in Trametes versicolor [121 130]The addition of veratryl alcohol to cultivation media of manywhite-rot fungi has resulted in an increase in laccase pro-duction [124 130] The aromatic compound hydroquinoneincreased 3-fold T versicolor laccase activity while decreas-ing 2- and 8-fold yields of MnP and endoglucanase [131]Hadibarata et al [132] have proved the importance of extra-cellular laccase of Armillaria sp F022 in the transformationof anthracene into anthraquinone benzoic acid and otherproducts such as 2-hydroxy-3-naphthoic acid and coumarin

46 Influence of Amino Acids on Laccase Production Lac-case production by white-rot fungi is strongly affected bythe presence of amino acids in the media [68] Variousamino acids and their analogues have shown stimulatory aswell as inhibitory effects on laccase production by Cyathusbulleri [133] According to this study DL-methionine DL-tryptophan glycine and DL-valine stimulated laccase pro-duction while L-cysteine monohydrochloride completelyinhibited the enzyme production Dong et al [68] usedamino acidmixture that contained the following amino acidsL-arginine L-histidine L-valine L-threonine L-isoleucineL-tyrosine L-methionine L-serine L-asparagine L-lysineL-aspartic acid L-tryptophan and L-cysteine at 1 (wv)concentration This amino acid mixture favoured the laccaseproduction by Trametes gallica It is possible that amino acidsact as inducer for laccase production bymanywhite-rot fungi[68 133] Sun et al [110] reported that all the six aminoacids (alanine histidine glycine arginine aspartate andphenylalanine) at 1mM concentration increase the catalyticability of the laccase enzyme from Ganoderma lucidumstrain 7071-9 when expressed in Pichia pastoris Amino acidtryptophan also induces laccase production in Crinipellis spRCK-1 [134]

47 Influence of Copper on Laccase Production Copper is anindispensable micronutrient for most living organisms andcopper requirements by microorganisms are usually satisfiedby low concentrations of the metal [105] In its free formcupric ion at higher concentration is extremely toxic tomicrobial cells The binding and uptake of copper in fungiusually comprise two phases metabolism-independent sur-face binding followed by an energy-dependent metal influx[135] The stimulatory effect of copper on laccase synthesiswas also effective for several other basidiomycetes and hencecould be used as a simple method to improve the productionof this enzyme [136] Using northern blot analysis it wasdetermined that increased production of laccase activitywould be obtained in the copper supplemented cultures ofPleurotus ostreatus [65]

Copper has been reported to be a strong laccase inducerin several species for example Neurospora crassa [137]Trametes versicolor [122] Phanerochaete chrysosporium [138]Panus osteratus [65] Pleurotus sajor-caju [123] Trametes

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

6 Enzyme Research

trogii [101] Volvariella volvacea [139] Lentinula edodes [104]and Grifola frondosa [105] Huber and Lerch [136] reportedthat Trametes pubescens grown at 20mM CuSO

4exhibited

high laccase activity (65UmL) and using western blotanalysis they further demonstrated that the synthesis of thelaccase protein was linked to the presence of copper ionsin the culture medium In addition both the time and theconcentration of copper supplementation were important forobtaining high levels of laccase According to a recent studyon the white-rot fungus Trametes trogii [101] the additionof copper strongly stimulated lignolytic enzyme productionand higher decolorization of polymeric dyes-poly R-478 wasobserved as well However higher copper concentrations(500mM) inhibited the growth and notably decreased man-ganese peroxidase production although they did not affectsecretion of laccase [101] The addition of low concentrationsof copper to the cultivation media of laccase producing fungistimulated laccase production [140] Palmieri et al [65] foundthat the addition of 150 120583Mcopper sulphate to the cultivationmedia can result in a fiftyfold increase in laccase activitycompared to a basal medium Copper has been reported tobe a strong laccase inducer in several species for exampleNeurospora crassa [136] Paecilomyces sp WSH-L07 [141]Shiraia bambusicola strainGZ11K2 [142]Trametes trogii TEMH2 [143] Pleurotus florida NCIM 1243 [106] Peniophora sp[144] and so forth

5 Laccases Inducers

The promoter regions of the genes encoding for laccase con-tain various recognition sites that are specific for xenobioticsand heavy metals [145] These xenobiotics and heavy metalscan bind to the recognition sites of the gene when present inthe medium and induce laccase production White-rot fungiwere very diverse in their responses to tested inducers forlaccase The addition of certain inducers can increase theconcentration of a specific laccase or induce the productionof new isoforms of the enzyme [146] Some inducers interactvariably with different fungal strains Lu et al [147] found thatthe addition of xylidine as inducer had the most pronouncedeffect on laccase production The addition of 10 120583M xylidineafter 24 h of cultivation gave the highest induction of laccaseactivity and increased laccase activity by ninefold At higherconcentrations the xylidine had a reduced effect probably dueto toxicity Laccase offers protection for the fungus againsttoxic phenolic monomers of polyphenols [147] Dhawan andKuhad [127] investigated the inducing effect of alcohols onthe laccase production by Trametes versicolor The enhancedlaccase activity was comparable to those obtained using 25-xylidine and veratryl alcohol [74] It was hypothesizedthat the addition of ethanol to the cultivation mediumcaused a reduction in melanin formation The monomerswhen not polymerised to melanin then acted as inducersfor laccase production [127] The addition of ethanol as anindirect inducer of laccase activity offers a very economicalway to enhance laccase production Garzillo et al [148]found that there was a strong correlation between hyphalbranching and the expression and secretion of laccase Theaddition of cellobiose can induce profuse branching in certain

Pycnoporus species and consequently increase laccase activity[148] The addition of cellobiose and lignin can increase theactivity of extracellular laccases without an increase in totalprotein concentration [149]

An important distinctionmay be drawnbetween laccasestheymay either be inducible or constitutively expressed [150]The constitutive or noninducible group does not react read-ily to dissolved compounds that exhibit properties similarto their substrates and no inducer producing significantimprovements in their yield has as yet been isolated Singleinducers may not elicit the desired response in laccase pro-duction and a complex mixture of inducers may be required[151]

Several compounds may elicit a positive response onlaccase production these compounds known as inducerswhich include the metal ions copper or cadmium [114]cycloheximide [152] and low molecular weight aromatic ororganic acids such as veratric acid [122] and ferulic acid[153] as well as other phenolic or aromatic compounds suchas 2 5-xylidine [154] and veratryl alcohol [155] Soden andDobson [122] proved that Cu2+ ions have the ability to inducelaccase production by forming an integral prosthetic groupIn the sameway natural substrates such as aromaticphenoliccompounds and lignin derivatives such as veratryl alcoholand 2 5-xylidine induced laccase production [53] Thereis evidence in Trametes versicolor that these compoundscause an increase in mRNA levels but only copper wasinvolved in increasing laccase mRNA translation [122] Theexact action of inducers is however unknown It has beendemonstrated that fungi may possess several isozymes oflaccase encoded by several laccase genes and these may bedifferentially regulated [122] It has further been suggestedthat the action of certain inducers may be a direct resultof their toxicity to the fungus and the capability of laccaseto polymerize and detoxify them [156] The use of inducersdoes however suffer from several disadvantages includingtheir toxicity and the extra expense associated with theaddition of an inducer The white-rot fungus Trametes spAH28-2 can synthesize extracellular laccase by induction incellobiose-based liquid culturemedium [157] Both yields andcomposition of laccase isoenzymes produced by Trametes spAH28-2 would be quite different with induction by differentsmall-molecule aromatic compounds o-toluidine guaiacoland 3 5-dihydroxytoluene which affected microbial growthand the synthesis of laccase isoenzymes differentially [157]

It has been suggested that the addition of veratryl alcoholmay not elicit an inductive effect rather it may act as a pro-tective agent against inactivation by hydrogen peroxideproduced endogenously by the fungus [158] thereby indi-rectly eliciting a higher enzyme production The additionof surfactants or detergents for example Tween 20 or 80has resulted in higher yields of ligninolytic enzymes incertain fungi There is evidence that these detergents resultin higher permeability of oxygen and extracellular enzymetransport through the cellmembranes of fungi [159] Effectiveinduction of laccase from Pleurotus florida with anionic andcationic surfactants has been demonstrated [160]

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 7

In spite of an initial inhibitory effect on mycelial growthethanol was shown to be a very strong inducer for laccaseexpression by Pycnoporus cinnabarinus [161] Shankar andShikha [144] reported that veratryl alcohol induced maxi-mum laccase production giving 607UmL laccase activityby Peniophora sp whereas 05mM xylidine was used asan inducer to optimized production of laccase by Coriolop-sis caperata RCK2011 under solid state fermentation [162]Xylidine is the most widely reported inducer of laccaseproduction and enhanced laccase specific production by 4-fold in Coriolopsis polyzona [163]

There have been many studies regarding the effects ofinducers using a plethora of fungal genera species andeven strains Differences in laccase stimulation were alreadyobserved in very early studies more than half a century agoEthanol has improved laccase synthesis significantly whenused as a carbon source [160] for a monokaryotic strainPycnoporus cinnabarinus Later work by this group indicatedthat ethanol improved gene expression and inhibited proteaseactivity thereby playing an important regulatory role inlaccase production by the fungus [164]

6 Purification and BiochemicalProperties of Laccases

Production of extracellular laccase is a common feature ofmany fungi particularly those associated with wood decayor the terminal stages of decomposition of leaf litter Currentknowledge about the structure and biochemical propertiesof fungal laccase proteins is based on the study of purifiedproteins More than 100 laccases from various fungi havebeen purified and characterized by researchers for morethan 35 years [10] Most of the white-rot fungi producelaccase in multiple isoforms [65] Several purification stepsare required to obtain a preparation free of both pigment andother contaminant proteinsMultiple steps like ultrafiltrationprecipitation using ammonium sulphate or organic solventsand ion exchange and size exclusion chromatography havebeen used for the purification of laccases from the culturefiltrate Typical fungal laccase is a protein of approximately60ndash70 kDa with acidic isoelectric point around 40 [10]

Several laccase isoenzymes have been detected in manyfungal species More than one isoenzyme is produced inmost white-rot fungi [165] This has been demonstratedby p-phenylenediamine staining the laccase activity in alltested wood rot fungi after isoelectric focusing All testedspecies namely Coprinus plicatilis Fomes fomentarius Het-erobasidion annosum Hypholoma fasciculare Kuehneromycesmutabilis Leptoporus litschaueri Panus stipticus Phellinusigniarius Pleurotus corticatus P ostreatus Polyporus bru-malis Stereum hirsutum Trametes gibbosa T hirsuta andT versicolor exhibited the production of more than oneisoenzyme typically with pI in the range of pH 3 to 5 [10]Thewhite-rot fungus P ostreatus produces at least eight differentlaccase isoenzymes six of which have been isolated andcharacterized [166 167] The production of laccase isoen-zymes in P ostreatus is regulated by the presence of copperand the two dimeric isoenzymes have only been detected

in the presence of copper [167] Isoenzymes of laccase withdifferent molecular weight and pI were also detected in thelitter-decomposing fungus Marasmius quercophilus [168] Astudy with 17 different isolates of this fungus showed that theisoenzyme pattern was consistent within different isolatesMoreover all isolates showed the same isoenzyme pattern(one of the three laccase bands on SDS PAGE) after inductionof laccase with different aromatic compounds [169]

The catalytic action of an enzyme is quantitativelydescribed by the Michaelis constant 119870

119872and the catalytic

efficiency constant 119896cat These constants have been measuredfor a large number of laccases and rather great variance canbe observed among them (Table 1)The119870

119872values of laccases

are generally in the range of 25120583Mdepending on the enzymesource and the reducing substrate (Table 1) The lowest 119870

119872

values have been measured with syringaldazine which is adimer of two molecules of 2 6-dimethoxyphenol linked byan azide bridge Either the azide bridge or the dimer formis apparently beneficial for the affinity of syringaldazine tolaccases because the 119870

119872values measured for monomeric 2

6-dimethoxyphenol are generally higher than those obtainedwith syringaldazine (Table 1) The comparison of 119870

119872values

also shows that laccases from different source organismshave different substrate preferences [170] The specificity foroxygen is less dependent on the enzyme and 119870

119872values

of 20ndash50120583M for O2have been reported for several laccases

[171 172]Very significant variance has also been observed in the

catalytic efficiencies (119896cat) of various laccases Differences ashigh as 3500-fold can be seen in the 119896cat values betweendifferent laccases with the same substrates (Table 1) On theother hand the 119896cat values for a single laccase do not generallydiffer more than 2ndash10-fold between different substrateswhich reflects the fact that 119896cat describes the rate of theelectron-transfer reactions taking place inside the enzymeafter substrate binding [172] However the variance in assayconditions must always be taken into account when thecatalytic constants measured in different laboratories arecompared The constants in Table 1 have been measuredunder varying pH ionic strength and temperature condi-tions and by using different protein concentrations all ofwhich have a great effect on the results In addition differentmolar extinction coefficients for oxidation products havesometimes been used in spectrophotometric assays becausethe nature of the actual oxidation products is often complexor poorly understood This affects particularly the numericalvalues of 119896cat

In addition to the kinetic constants the catalytic per-formance of laccases by catalytic activity and stability indifferent pH and temperature conditions has been describedThe pH activity profiles of laccases are often bell-shapedwith optima around 46 when measured with phenolicsubstrates [50] The decrease in laccase activity in neutral oralkaline pH values is affected by increasing hydroxide anioninhibition because as a small anion hydroxide ion is also alaccase inhibitor On the other hand increasing pH decreasesthe redox potential of the phenolic substrate making thesubstrate more susceptible to oxidation by laccase [173]Oxidation of nonphenolic substrates such as ABTS does not

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

8 Enzyme Research

Table 1 Kinetic constants of laccases at specified pH

Substrate 119870119872

119896cat pH Laccase Reference(M) (minminus1)

Guaiacol

1200 150 6 Pleurotus ostreatus POXC [165]3100 nrlowast 6 Pleurotus ostreatus POXA2 [165]400 nr 6 Chaetomium thermophilum [174]5120 115 34 Trametes trogii POXL3 [148]510 nr 45 Gaeumannomyces graminis [249]36 10800 3 Trametes pubescens LAP2 [181]66 6800 65 Pleurotus sajor-caju Lac4 [185]

ABTS

58 2700 53 Trametes villosa Lcc1 [169]52 nr 53 Rhizoctonia solani Lcc4 [169]90 350000 3 Pleurotus ostreatus POXA1 [165]120 nr 3 Pleurotus ostreatus POXA2 [165]280 57000 3 Pleurotus ostreatus POXC [165]190 nr 6 Chaetomium thermophilum [174]30 198 34 Trametes trogii POXL3 [148]32 nr 3 Panaeolus sphinctrinus [83]41 nr 5 Coprinus friesii [83]23 1090 55 Coprinus cinereus Lcc1 [50]14 41400 3 Trametes pubescens LAP2 [81]45 620 55 Trichophyton rubrum [175]55 nr 4 Pycnoporus cinnabarinus [184]

2500 74000 33 Pleurotus sajor-caju Lac4 [185]290 790 6 Myceliophthora thermophila [196]

Syringalda-zine

39 3000 53 Trametes villosa Lcc1 [169]28 nr 53 Rhizoctonia solani Lcc4 [169]20 23000 6 Pleurotus ostreatus POXC [165]130 28000 6 Pleurotus ostreatus POXA1 [165]140 nr 6 Pleurotus ostreatus POXA2 [165]34 nr 6 Chaetomium thermophilum [174]26 180 55 Coprinus cinereus Lcc1 [50]6 16800 45 Trametes pubescens LAP2 [181]280 35000 65 Pleurotus sajor-caju Lac4 [185]16 2100 6 Myceliophthora thermophila [196]

26-DMP

100 nr 35 Botrytis cinerea [251]230 430 5 Pleurotus ostreatus POXC [165]2100 21000 5 Pleurotus ostreatus POXA1 [165]740 nr 65 Pleurotus ostreatus POXA2 [165]410 109 34 Trametes trogii POXL3 [148]96 nr 6 Chaetomium thermophilum [174]26 nr 45 Gaeumannomyces graminis [249]72 24000 3 Trametes pubescens LAP2 [181]120 58000 6 Pleurotus sajor-caju Lac4 [185]

lowastnr not reportedABTS 221015840-azinobis-(3-ethylbenzthiazoline-6-sulphonate)26-DMP 26-dimethoxyphenol

involve proton exchange and therefore nearly monotonic pHactivity profiles with highest activities at pH values of 23 areobtained [174] In contrast to their activity the stability oflaccases is generally the highest at pH values around 8-9 [170

175] Temperature stabilities of laccases vary considerablydepending on the source organism In general laccases arestable at 30ndash50∘C and rapidly lose activity at temperaturesabove 60∘C [176 177]

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 9

Table 2 Laccase genes that have been shown to encode a biochemically characterized laccase protein [252]

OrganismGene Protein encoded by the gene

Name E MBL Length MW+pI

Acc Number (aa)lowastlowast (kDa)Ceriporiopsis subvermispora lcs-1 AY219235 519 79 36Coprinus cinereus lcc1 AF118267 539 63 37ndash40Cryptococcus neoformans CNLAC1 L22866 624 75 ndlowast

Gaeumannomyces graminis LAC2 AJ417686 577 70 56Marasmius quercophilus lac1 AF162785 517 62 36Myceliophthora thermophila lcc1 AR023901 619 80 42Neurospora crassa 2 alleles M18333-4 619 64 68Phlebia radiata X52134 lac1 mdash 548 64 35Pleurotus ostreatus poxa1b AJ005017 533 62 69Pleurotus ostreatus poxc Z49075 533 67 47Basidiomycete PM1(CECT2971) lac1 Z12156 517 64 36Podospora anserina lac2 Y08827 621 70 710Populus euramericana lac90 Y13772 574 90 92Rhizoctonia solani lcc4 Z54277 530 66 75Streptomyces lavendulae mdash AB092576 631 73 ndlowast

Trametes pubescens lap2 AF414807 523 65 26Trametes trogii lcc1 Y18012 496 70 33ndash36Trametes versicolor lccI L49376 519 67 ndlowast

Trametes versicolor lcc2 U44430 520 64 31ndash33Trametes villosa lcc1 L49377 520 63 35Trametes villosa lcc2 AY249052 519 63 62ndash68lowastnd not determined+Molecular weights determined by SDS-PAGElowastlowastAmino acids

7 Molecular Biology of Laccases

The first laccase genes were isolated and sequenced about 18years ago from the fungi Neurospora crassa [178] Aspergillusnidulans [179 180] and Phlebia radiata [181] Since thensequencing of laccase genes has increased considerably How-ever the number of laccase genes of which the correspondingprotein products have been experimentally characterized issignificantly lower To date there are about 20 such enzymesmost of which are fungal laccases (Table 2) A typical laccasegene codes for a protein of 500ndash600 amino acids and themolecular weights of laccases are usually in the range of 60 to90 kDa when determined by SDS-PAGE (Table 2) Differencebetween the molecular weight predicted from the peptidesequence and the experimentally obtained molecular weightis caused by glycosylation which typically accounts for about10ndash20 of the total MW [182] The isoelectric points ofmicrobial laccases are generally around 36 (Table 2) Severalfungal genomes contain more than one laccase gene [121]The expression levels of different laccase genes typicallydepend on cultivation conditions [123] For example highnitrogen content of the medium has been shown to inducetranscription of laccase genes in the Basidiomycete I-62(CECT 20197) and in Pleurotus sajor-caju [123]

Copper is also often a strong inducer of laccase genetranscription and this has been suggested to be related to

a defense mechanism against oxidative stress caused by freecopper ions [182] In addition to copper other metal ionssuch as Mg2+ Cd2+ or Hg2+ can also stimulate laccase exp-ression [182] Certain aromatic compounds that are struc-turally related to lignin precursors such as 2 5-xylidine orferulic acid have also been shown to increase laccase genetranscription in Trametes villosa Trametes versicolor andPleurotus sajor-caju [123] On the other handTrametes villosaand Pleurotus sajor-caju have also been shown to containconstitutively expressed laccase genes and thismay be relatedto different physiological roles of the various laccases in thefungi [123] A clear understanding of expression laccase genemay lead to overproduction of laccase enzyme

71 Heterologous Production of Laccases The natural hostsproduce very low yields of laccases for commercial pur-poses Therefore to improve the production the cloningof laccase gens and heterologous expression are employedRecent advances in the field of genetic engineering haveallowed the development of efficient expression vectors forthe production of functional laccase Laccase genewas clonedin the most commonly used organisms Pichia pastoris [183]Aspergillus oryzae [184] A niger [185 186] A nidulans [187]Trichoderma reesei [188] and Yarrowia lipolitica [189] Lac-case production levels have often been improved significantly

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

10 Enzyme Research

Table 3 Laccase production in heterologous hosts [252]

Laccase gene Production host Laccase production (mgLminus1)lowast

Ceriporiopsis subvermispora lcs-1 Aspergillus nidulans 15Aspergillus niger 15

Coprinus cinereus lcc1 Aspergillus oryzae 135

Myceliophthora thermophila lcc1 Aspergillus oryzae 19Saccharomyces cerevisiae 18

Phlebia radiata lac1 Trichoderma reesei 20

Pleurotus sajor-caju lac4 Pichia pastoris 49

Pycnoporus cinnabarinus lac1Pichia pastoris 8Aspergillus niger 70Aspergillus oryzae 80

lowastThe reported production levels have been obtained in shake flask cultivations except in the case of Phlebia radiata laccase which was produced in a laboratoryfermentor

by expression in heterologous hosts but the reported levelshave still been rather low for industrial applications (Table 3)The common problems associated with heterologous expres-sion of fungal enzymes are incorrect folding and inefficientcodon usage of expression organisms resulting in nonfunc-tional or low yields of enzyme The incorrect substitution ofcarbohydrate residues during glycosylation of proteins whichis due to preferential utilization of specific carbohydrates bythe expression organism may pose an additional problem toheterologous expressionThese problems are being overcomeby using more advanced organisms as expression vectorswhose codon usage and molecular folding apparatus aresuitable for correct expression of these proteins

Production of heterologous laccase has often been impro-ved by varying the cultivation conditions For example betterproduction of heterologous laccase has been achieved in yeastsystems by controlling the pH of the culture medium andby lowering cultivation temperatures [190 191] Buffering ofthe culture medium to maintain the pH above 4 has beenproposed to be important in stability of secreted laccasesand inactivation of acidic proteases [190] whereas loweredcultivation temperatures may result in better production dueto improved folding of heterologous proteins [192] In addi-tion over expression of Sso2p a membrane protein involvedin the protein secretion machinery [192] Larsson et al hasbeen shown to improve heterologous laccase production inS cerevisiae [193 194]

The addition of copper to the culture medium has alsoproved to be important for heterologous laccase productionin Pichia pastoris and Aspergillus sp [191 195] In contrast tohomologous laccase production in which copper additionoften affects laccase gene expression the increased laccaseproduction by copper addition is probably related to improv-ing folding of the active laccase in heterologous production[195] The importance of adequate copper concentration forproper laccase folding was further corroborated by studiesin which two genes related to copper-trafficking in Trametesversicolor were overexpressed in S cerevisiae expressing Tversicolor lacIII gene the heterologous laccase production byS cerevisiae was improved up to 20-fold [196] The effect was

suggested to result frommore efficient transport of copper tothe Golgi compartment [196]

Directed evolution has also been used for improvingheterologous laccase production Mutations in the Myce-liophthora thermophila laccase gene resulted in the high-est reported laccase production level in S cerevisiae [197]The most important obstacles to commercial application oflaccases are the lack of sufficient enzyme stocks and thecost of redox mediators Thus efforts have to be made inorder to achieve cheap overproduction of these biocatalystsin heterologous hosts and also theirmodification by chemicalmeans of protein engineering to obtain more robust andactive enzymes

8 Mode of Action

Laccases are mostly extracellular glycoproteins [83] and aremultinuclear enzymes [69] with molecular weights between60 and 80 kDa [83] Most monomeric laccase moleculescontain four copper atoms in their structure that can beclassified in three groups using UVvisible and electronparamagnetic resonance (EPR) spectroscopy [198] The typeI copper (T1) is responsible for the intense blue colour ofthe enzymes at 600 nm and is EPR-detectable the type IIcopper (T2) is colourless but is EPR-detectable and the typeIII copper (T3) consists of a pair of copper atoms that give aweak absorbance near the UV spectrum but no EPR signal[199]The T2 and T3 copper sites are close together and forma trinuclear centre [198] that are involved in the catalyticmechanism of the enzyme [199]

Laccase only attacks the phenolic subunits of lignin lead-ing to C120572 oxidation C120572-C120573 cleavage and aryl-alkyl cleavageLaccases are able to reduce one molecule of dioxygen to twomolecules of water while performing one-electron oxidationof a wide range of aromatic compounds [8] which includespolyphenols [200] methoxy-substituted monophenols andaromatic amines [201] This oxidation results in an oxygen-centred free radical which can then be converted into asecond enzyme-catalysed reaction to quinone The quinoneand the free radicals can then undergo polymerization [8]

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 11

Laccases are similar to other phenol-oxidising enzymeswhich preferably polymerise lignin by coupling of the phe-noxy radicals produced from oxidation of lignin phenolicgroups [202] Due to this specificity for phenolic subunitsin lignin and their restricted access to lignin in the fibrewall laccase has a limited effect on pulp bleaching [200] Thesubstrate range of laccase can be extended to nonphenolicsubunits of lignin by the inclusion of a mediator such as 221015840-azinobis-(3-ethylbenzthiazoline-6-sulfonate) (ABTS)

9 Biotechnological Applications of Laccase

Laccases of fungi are of particular interest with regard topotential industrial applications because of their capabilityto oxidize a wide range of industrially relevant substratesOxidation reactions are comprehensively used in industrialprocesses for instance in the textile food wood process-ing and pharmaceutical and chemical industries Enzymaticoxidation is a potential substitute to chemical methods sinceenzymes are very specific and efficient catalysts and areecologically sustainable Laccases are currently studied inten-sively formany applications and they are already used in largescale in the textile industry Together with low molecularweight redox-mediator compounds laccases can generate adesired worn appearance on denim by bleaching indigo dye[203] The potential use of laccase for bleaching has beeninvestigated and this has even led to the esoteric suggestionof using laccase in the presence of hydroxyl stilbenes ashair dyes [204] Another potential environmental applicationfor laccases is the bioremediation of contaminated soils aslaccases are able to oxidize toxic organic pollutants such aspolycyclic aromatic hydrocarbons [205] and chlorophenols[150] The most useful method for this application wouldprobably be inoculating the soil with fungi that are efficientlaccaseproducers because the use of isolated enzymes is noteconomically feasible for soil remediation in large scale Thecurrent practical applications of the use of laccase have ledto a search for source of the enzyme from white-rot fungiand the use of mediators which promote or facilitate enzymeaction

10 Laccases Role in Bioremediation

One of themajor environmental problems faced by theworldtoday is the contamination of soil water and air by toxicchemicals With industrialization and the extensive use ofpesticides in agriculture the pollution of the environmentwith mandate organic compounds has become a seriousproblem Eighty billion pounds of hazardous organopo-llutants are produced annually in the United States and only10 of these are disposed of safely [206] Certain hazardouscompounds such as polycyclic aromatic hydrocarbons(PAH) pentachlorophenols (PCP) polychlorinated biphe-nyls (PCB) 111-trichloro-22-bis(4-chlorophenyl) ethane(DDT) benzene toluene ethylbenzene and xylene (BTEX)as well as trinitrotoluene (TNT) are persistent in the env-ironment and are known to have carcinogenic andormutanogenic effects The ability of fungi to transform

a wide variety of hazardous chemicals has aroused interest inusing them in bioremediation [207] Enzymatic treatment iscurrently considered an alternative method for the removalof toxic xenobiotics from the environment [150]

101 Degradation of Xenobiotics Laccases exhibit broad sub-strate specificity and is thus able to oxidize a broad rangeof xenobiotic compounds including chlorinated phenolics[208] pesticides [209] and polycyclic aromatic hydrocarbons[210] Moreover polycyclic aromatic hydrocarbons whicharise from natural oil deposits and utilization of fossilfuels were also found to be degraded by laccases [211]Laccase purified from a strain of Coriolopsis gallica oxidizedcarbozoleN-ethylcarbozole fluorine and dibenzothiophenein presence of 1-hydroxybenzotriazole and 221015840-azinobis (3-ethylbenzthiazoline)-6-sulfonic acid as free radicalmediators[212] Laboratory experiments have demonstrated that phe-nols and aromatic amines may be removed from water bythe application of laccase [213] The underlying mechanismof the removal involves enzymatic oxidation of the pollutantsto free radicals or quinones that undergo polymerization andpartial precipitation [213] Laccase from white-rot fungusTrametes hirsuta has been used to oxidize alkenes [214] Theoxidation is the effect of a two-step process in which theenzyme first catalysed the oxidation of primary substratea mediator added to the reaction and then the oxidizedmediator oxidizes the secondary substrate the alkene to thecorresponding ketone or aldehyde In addition to substrateoxidation laccase can also immobilize soil pollutants bycoupling to soil humic substancesmdasha process analogous tohumic acid synthesis in soils [215] The xenobiotics that canbe immobilized in this way include phenolic compoundsincluding chlorinated phenols and anilines such as 3 4-dichloroaniline 2 4 6-trinitrotoluene or chlorinated phe-nols [216] The immobilization lowers the biological avail-ability of the xenobiotics and thus their toxicity A laccaseproduced in the yeast Pichia pastoris was engineered by site-directed mutagenesis to improve the rate of electron transferbetween the copper-containing active site of laccase and anelectrode [217] Thus laccase may be usefully engineeredto improve the efficiency of particular bioremediation pro-cesses

102 Decolourisation of Dyes The textile industry accountsfor two-thirds of the total dyestuff market and consumeslarge volumes of water and chemicals for wet processing oftextiles [218] The chemical reagents used are very diverse inchemical composition ranging from inorganic compoundsto polymers and organic products [219] There are about100000 commercially available dyes with over 7 times 105 tonnesof dyestuff produced annually [220] Due to their chemicalstructure dyes are resistant to fading on exposure to lightwater and different chemicals and most of them are difficultto decolourise due to their synthetic origin

Government legislation is becoming more and morestringent especially in themore developed countries regard-ing the removal of dyes from industrial effluents [221] Con-cern arises as several dyes are made from known carcinogens

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

12 Enzyme Research

such as benzidine and other aromatic compounds [222]Most currently existing processes to treat dye wastewater areineffective and not economical Therefore the developmentof processes based on laccases seems an attractive solutiondue to their potential in degrading dyes of diverse chemicalstructure [223] including synthetic dyes currently employedin the industry [224] The use of laccase in the textileindustry is growing very fast since besides decolorizingtextile effluents as commented above laccase is used to bleachtextiles and even to synthesize dyes [225] Flavodon flavusdecolourized several synthetic dyes such as Azure B andBrilliant Blue R in low nitrogen medium [226] Alternativelylaccase along with stabilizers may be suitable for treatmentof wastewater [227 228] Partial decolorization of two azodyes and complete decolorization of two triphenylmethanedyes (bromophenol blue and malachite green) was achievedby cultures ofPycnoporus sanguineus producing laccase as thesole phenoloxidase [120 229] Saratale et al [230] demon-strated employing HPLC analysis the degradation of the dyeldquoNavy blueHERrdquo by fungusTrichosporon beigeliiNCIM-3326after one day under static conditions for the identificationof metabolic products from dye degradation Enayatizamiret al [231] observed degradation of 92 in the Azo BlackReactive 5 dye by P chrysosporium after 3 days of treatmentP chrysosporiumURM6181 andCurvularia lunataURM6179strains decolourize effluent containing textile indigo dye byapproximately 95 for 10 days of treatment [232] Laccasepurified from the fungusTrametes hirsutawas able to degradetriarylmethane indigoid azo and athraquinonic dyes used indyeing textiles [233] as well as 23 industrial dyes [234]

103 Effluent Treatment Laccases from fungi offer severaladvantages of great interest to biotechnological applicationsof industrial effluent treatment As they exhibit broad sub-strate specificity they can bleach Kraft pulp or detoxifyagricultural byproducts including olive mill wastes or coffeepulp [235] Laccase of an isolate of the fungus Flavodonflavus was shown to decolourize the effluent from a Kraftpaper mill bleach plant [226] Laccase purified from white-rot basidiomycete Trametes villosa degrades bisphenol Aan endocrine-disrupting chemical [225] Nonylphenols haveincreasingly gained attention because of their potential tomimic the action of natural hormones in vertebrates [236]They result from incomplete biodegradation of nonylphenolpolyethoxylates (NPEOs) which have been widely used asnonionic surfactants in industrial processes Both nonylphe-nols andNPEOs are discharged into the environmentmainlydue to incomplete removal of wastewater treatment facilities[236] Nonylphenols are more resistant to biodegradationthan their parent compound and hence are found worldwidein wastewater treatment plant effluents and rivers [237] Dueto their hydrophobicity they tend to be absorbed onto surfacewater particles and sediments and accumulate in aquaticorganisms Consequently nonylphenols represent a seriousenvironmental and human health risk Laccases from aquatichyphomycete Clavariopsis aquatica have proved to degradexenoestrogen nonylphenol [238] In addition to the potentialrole of such degradation processes for natural attenuationprocesses in freshwater environments this enzyme laccase

also offers new perspectives for biotechnological applicationssuch as wastewater treatment

104 Laccases Pulp and Paper Pulp bleaching is currentlyachieved by treating pulps with chlorine-based chemicalsThis results in the formation of chlorinated aliphatic and aro-matic compounds that could be acutely toxic mutagenic andcarcinogenic [239] In recent years there have been intensivestudies performed to develop enzymatic environmentallybenign bleaching technologies [239] The use of laccase-mediated systems has shown potential for the biobleachingof pulp but the feasibility of its use is hindered by the lackof an inexpensive mediator [239] The bioremediatory roleof laccases in the pulp and paper industry is hindered by thealkalinity of the effluent Thus several researchers have spentconsiderable effort in identifying laccases that could be suit-able for this type of remediationThe laccase fromCoriolopsisgallica has been implicated in the decolourisation of alkalineeffluents such as the effluent from the pulp and paper industry[240] Laccases have also been shown to be applicable to thebioremediation of pulp and paper industry waste by effectingdirect dechlorination [241] and the removal of chorophenolsand chlorolignins from bleach effluents [242] Other uses oflaccases for the pulp and paper industry include reductionof the kappa number of pulp [243] and an improvement inthe paper making properties of pulp [244] Fungal laccasescan be used for the treatment of effluents from pulp mills orfrom other industries containing chlorolignins or phenoliccompounds [245] Laccases render phenolic compounds lesstoxic via degradation or polymerization reactions andorcross-coupling of pollutant phenol with naturally occurringphenols [170]

105 Laccases Biosensors and Biofuel Cells Theuse of laccasein biosensor technology is mainly attributed to its broadsubstrate range allowing for the detection of a broad rangeof phenolics this does however disallow the detection ofspecific constituents [246 247] Biosensors that utilize laccaseinclude an electrode that may be used for the detection ofphenols such as catechols in tea [247] phenolic compoundsin wine and lignins and phenols in wastewaters [248]Fogel and Limson [246] developed a rapid simple methodof electrochemically predicting a given phenolic substratersquosability by amperometric laccase biosensors Novel biosensorshave been developed using beneficial properties of laccasesuch as the potentiometric immunosensor for the detectionof antigens [248] Laccase has displayed a significant potentialfor its use in biofuel cells [249] The major reason for thisinterest is the use of oxygen as a substrate which is convertedinto water The obvious advantage of this is the potential usein nanotechnology for medical applications in living animalssince oxygen may be scavenged from the bloodstream whilethe byproduct (water) is benign Slomczynski et al [250]developed a zinc-laccase biofuel cell adapting the zinc-aircell design configuration Unlike most biofuel cells this zinc-laccase cell operated under open ambient conditions In thissingle chamber membraneless cell design was utilized andlaccase biocatalyst was left to be freely suspended (ie not

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 13

immobilized) in quasineutral potassium dihydrogen phos-phate buffer (pH 65) electrolyte Despite its simple designfeatures and not operating under controlled conditions thezinc-laccase system studied demonstrated power output ofcomparable performance to biofuel cell system utilizing amuch more complex design immobilized enzyme and elec-tron transfer mediator controlled temperature and humidityoxygenated electrolyte and so forth [250] The drawbackof using laccase in this technology is its inability to reduceoxygen at the physiological pH of blood a technical hurdlethat must be overcome [251]

106 Food and Beverage Industry The beverage industry isalso set to be a benefactor of laccase Laccase may preventundesirable changes such as discoloration clouding hazeor flavour changes in beer fruit juices and wine improvingtheir shelf life by removing phenols such as coumaric acidsflavans and anthocyanins [150 251] The practical applica-tions of laccases have led to a search for sources of theenzyme fromwhite-rot fungi and the use of mediators whichpromote or facilitate enzyme actionThis review summarizesthe available data about the biological properties of fungallaccases their occurrence and biotechnological applicationsIt is clear from the forgone survey of literature that focushas been paid to a few laccase producing fungi particularlyPhanerochaete chrysosporium Trametes versicolor Pleurotusostreatus and so forth but there are still large numbersof fungal organisms not covered for laccase productionSearch and screening of uncovered fungal organisms areneeded along with the known and reference culture to selectthe potential culture with production of laccase in largeramounts Further understanding of kinetic parameters oflaccases will be useful to application of laccases for practicalpurposes

11 Conclusion

Because of their specific nature laccases are receiving muchattention from researchers around the globe The interestin utilizing laccases for biotechnological applications hasincreased rapidly since the discovery of these enzymes inwhite-rot fungi Emerging technologies include selectivedelignification for production of cellulosics in pulp bleachingconversion of lignocellulosics into feed and biofuel andtreatment of environmental pollutants and toxicants gen-erated in various industrial processes Therefore laccaseshave been widely studied for various applications includingthe functionalization of lignocellulosic materials wood fibermodification and the remediation of soil and contaminatedeffluents as well as their use in biosensors This review showsthat laccase has a great potential application in environmentprotectionHowevermuchmore research is required tomakeuse of laccases to protect environment and other industrialapplications

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of their paper

Acknowledgments

The corresponding author Buddolla Viswanath is thank-ful to Science and Engineering Research Board (SERB)Department of Science and Technology (DST) Governmentof India for awarding Young Scientist Scheme (SRFTLS-1442010) to the project entitled ldquoEnvironmental geochem-istry human in vitro bioaccessibility and ecosystem healtheffects of scarce technologically important metals (STIM)rdquoThe authors are all thankful to Professor Bontha RajasekharReddy SK University Anantapur India and other anony-mous reviewers for their valuable suggestions to improve thisreview

References

[1] B Viswanath M Subhosh Chandra H Pallavi and BRajasekhar Reddy ldquoScreening and assessment of laccase pro-ducing fungi isolated from different environmental samplesrdquoAfrican Journal of Biotechnology vol 7 no 8 pp 1129ndash11332008

[2] Shraddha R Shekher S Sehgal M Kamthania and A KumarldquoLaccase microbial sources production purification andpotential biotechnological applicationsrdquo Enzyme Research vol2011 Article ID 217861 11 pages 2011

[3] J M Bollag K L Shuttleworth and D H Anderson ldquoLaccase-mediated detoxification of phenolic compoundsrdquo Applied andEnvironmentalMicrobiology vol 54 no 12 pp 3086ndash3091 1988

[4] G Singh P Sharma and N Capalash ldquoPerformance of an alka-lophilic and halotolerant laccase from 120574-proteobacterium JB inthe presence of industrial pollutantsrdquo Journal of General andApplied Microbiology vol 55 no 4 pp 283ndash289 2009

[5] G Singh A Bhalla P Kaur N Capalash and P Sharma ldquoLac-case fromprokaryotes a new source for an old enzymerdquoReviewsin Environmental Science and Biotechnology vol 10 no 4 pp309ndash326 2011

[6] B Viswanath M S Chandra K P Kumar and B RajasekharReddy ldquoProduction and purification of laccase from Stereumostrea and its ability to decolorize textile dyesrdquo Dynamic Bio-chemistry Process BiotechnologyMolecular Biology vol 2 pp 19ndash25 2008

[7] Y Shi L chai C Tang et al ldquoCharacterization and gen-omic analysis of kraft lignin biodegradation by the beta-pro-teobacterium Cupriavidus basilensis B-8rdquo Biotechnology forBiofuels vol 6 p 1 2013

[8] C F Thurston ldquoThe structure and function of fungal laccasesrdquoMicrobiology vol 140 no 1 pp 19ndash26 1994

[9] S S Desai and C Nityanand ldquoMicrobial laccases and theirapplications a reviewrdquoAsian Journal of Biotechnology vol 3 no2 pp 98ndash124 2011

[10] P Baldrian ldquoFungal laccases-occurrence and propertiesrdquo FEMSMicrobiology Reviews vol 30 no 2 pp 215ndash242 2006

[11] J C Gonzalez S C Medina A Rodriguez J F Osma and CJ Almeciga-Diaz ldquoProduction of Trametes pubescens laccaseunder submerged and semi-Solid culture conditions on agro-Industrial wastesrdquo PLoS ONE vol 8 no 9 Article ID e737212013

[12] S Rodrıguez Couto and J L Toca Herrera ldquoIndustrial and bio-technological applications of laccases a reviewrdquo BiotechnologyAdvances vol 24 no 5 pp 500ndash513 2006

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

14 Enzyme Research

[13] R Sanchez A Ferrer L Serrano A Toledano J Labidi and ARodrıguez ldquoHesperaloe funifera as a raw material for integralutilization of its componentsrdquo BioResources vol 6 no 1 pp 3ndash21 2011

[14] R C Minussi M A Miranda J A Silva et al ldquoPurificationcharacterization and application of laccase from Trametes versi-color for colour and phenolic removal of olive mill wastewaterin the presence of 1-hydroxybenzotriazolerdquo African Journal ofBiotechnology vol 6 no 10 pp 1248ndash1254 2007

[15] S Riva ldquoLaccases blue enzymes for green chemistryrdquo Trends inBiotechnology vol 24 no 5 pp 219ndash226 2006

[16] G Bertrand ldquoSur la laccase et sur le pouvoir oxydant de cettediastaserdquo Comptes Rendus de LrsquoAcademie des Sciences vol 120pp 266ndash269 1985

[17] P RanochaGMcDougall SHawkins et al ldquoBiochemical char-acterization molecular cloning and expression of laccasesmdasha divergent gene familymdashin poplarrdquo European Journal of Bio-chemistry vol 259 no 1-2 pp 485ndash495 1999

[18] G L Woolery L Powers J Peisach and T G Spiro ldquoX-ray absorption study of Rhus laccase evidence for a copper-copper interactionwhich disappears on type 2 copper removalrdquoBiochemistry vol 23 no 15 pp 3428ndash3434 1984

[19] G Battistuzzi G Di Rocco A Leonardi andM Sola ldquo1HNMRof native and azide-inhibited laccase from Rhus verniciferardquoJournal of Inorganic Biochemistry vol 96 no 4 pp 503ndash5062003

[20] D L Johnson J LThompson S M Brinkmann K A Schullerand L L Martin ldquoElectrochemical characterization of purifiedRhus vernicifera laccase voltammetric evidence for a sequentialfour-electron transferrdquo Biochemistry vol 42 no 34 pp 10229ndash10237 2003

[21] B Gavnholt and K Larsen ldquoMolecular biology of plant laccasesin relation to lignin formationrdquo Physiologia Plantarum vol 116no 3 pp 273ndash280 2002

[22] J T Hoopes and J F D Dean ldquoFerroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipiferardquo PlantPhysiology and Biochemistry vol 42 no 1 pp 27ndash33 2004

[23] A De Marco and K A Roubelakis-Angelakis ldquoLaccase activitycould contribute to cell-wall reconstitution in regeneratingprotoplastsrdquo Phytochemistry vol 46 no 3 pp 421ndash425 1997

[24] A M Mayer and R C Staples ldquoLaccase new functions for anold enzymerdquo Phytochemistry vol 60 no 6 pp 551ndash565 2002

[25] S F Moin and M N Omar ldquoLaccase enzymes purificationstructure to catalysis and tailoringrdquo Protein Peptide Letters vol20 no 12 2013

[26] A Givaudan A Effosse D Faure P Potier M-L Bouillantand R Bally ldquoPolyphenol oxidase in Azospirillum lipoferumisolated from rice rhizosphere evidence for laccase activity innon-motile strains of Azospirillum lipoferumrdquo FEMSMicrobiol-ogy Letters vol 108 no 2 pp 205ndash210 1993

[27] D FaureM L Bouillant andR Bally ldquoIsolation ofAzospirillumlipoferum 4T Tn5 mutants affected in melanization and laccaseactivityrdquo Applied and Environmental Microbiology vol 60 no9 pp 3413ndash3415 1994

[28] A Sanchez-Amat P Lucas-Elıo E Fernandez J C Garcıa-Borron and F Solano ldquoMolecular cloning and functionalcharacterization of a unique multipotent polyphenol oxidasefrom Marinomonas mediterraneardquo Biochimica et BiophysicaActa vol 1547 no 1 pp 104ndash116 2001

[29] L OMartins CM Soares MM Pereira et al ldquoMolecular andbiochemical characterization of a highly stable bacterial laccase

that occurs as a structural component of the Bacillus subtilisendospore coatrdquo Journal of Biological Chemistry vol 277 no 21pp 18849ndash18859 2002

[30] M E Arias M Arenas J Rodrıguez J Soliveri A S Ball andM Hernandez ldquoKraft pulp biobleaching and mediated oxida-tion of a nonphenolic substrate by laccase from Streptomycescyaneus CECT 3335rdquo Applied and Environmental Microbiologyvol 69 no 4 pp 1953ndash1958 2003

[31] T Suzuki K Endo M Ito H Tsujibo K Miyamoto and YInamori ldquoA thermostable laccase from Streptomyces lavendulaeREN-7 purification characterization nucleotide sequence andexpressionrdquo Bioscience Biotechnology and Biochemistry vol 67no 10 pp 2167ndash2175 2003

[32] H Claus ldquoLaccases and their occurrence in prokaryotesrdquoArchives of Microbiology vol 179 no 3 pp 145ndash150 2003

[33] A B Dalfard K Khajeh M R Soudi H Naderi-Manesh BRanjbar and R H Sajedi ldquoIsolation and biochemical charac-terization of laccase and tyrosinase activities in a novel melan-ogenic soil bacteriumrdquo Enzyme and Microbial Technology vol39 no 7 pp 1409ndash1416 2006

[34] K Koschorreck S M Richter A B Ene E Roduner R DSchmid and V B Urlacher ldquoCloning and characterization of anew laccase from Bacillus licheniformis catalyzing dimerizationof phenolic acidsrdquo Applied Microbiology and Biotechnology vol79 no 2 pp 217ndash224 2008

[35] G Naclerio A Falasca E Petrella V Nerone F Cocco and FCelico ldquoPotential role of Bacillus endospores in soil amended byolivemill wastewaterrdquoWater Science and Technology vol 61 no11 pp 2873ndash2879 2010

[36] L-L Kiiskinen L Viikari andK Kruus ldquoPurification and char-acterisation of a novel laccase from the ascomyceteMelanocar-pus albomycesrdquoApplied Microbiology and Biotechnology vol 59no 2-3 pp 198ndash204 2002

[37] Y Kim N-S Cho T-J Eom and W Shin ldquoPurification andcharacterization of a laccase from Cerrena unicolor and itsreactivity in lignin degradationrdquoBulletin of the KoreanChemicalSociety vol 23 no 7 pp 985ndash989 2002

[38] G Iyer and B B Chattoo ldquoPurification and characterization oflaccase from the rice blast fungus Magnaporthe griseardquo FEMSMicrobiology Letters vol 227 no 1 pp 121ndash126 2003

[39] A Levasseur M Saloheimo D Navarro et al ldquoExploringlaccase-like multicopper oxidase genes from the ascomyceteTrichoderma reesei a functional phylogenetic and evolutionarystudyrdquo BMC Biochemistry vol 11 no 1 article 32 2010

[40] D H Nghi B Bittner H Kellner et al ldquoThe Wood Rot Asc-omycete Xylaria polymorpha produces a novel GH78 glycosidehydrolase that exhibits L-Rhamnosidase and feruloyl esteraseactivities and releases hydroxycinnamic acids from lignocellu-losesrdquo Applied Environmental Microbiology vol 78 no 14 p4893 2012

[41] M Scherer and R Fischer ldquoPurification and characterization oflaccase II of Aspergillus nidulansrdquo Archives of Microbiology vol170 no 2 pp 78ndash84 1998

[42] C Junghanns M Moeder G Krauss C Martin and DSchlosser ldquoDegradation of the xenoestrogen nonylphenol byaquatic fungi and their laccasesrdquo Microbiology vol 151 no 1pp 45ndash57 2005

[43] M De Jesus A M Nicola M L Rodrigues G Janbon and ACasadevall ldquoCapsular localization of the Cryptococcus neofor-mans polysaccharide component galactoxylomannanrdquo Eukary-otic Cell vol 8 no 1 pp 96ndash103 2009

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 15

[44] R Ikeda T Sugita E S Jacobson and T Shinoda ldquoEffectsof melanin upon susceptibility of Cryptococcus to antifungalsrdquoMicrobiology and Immunology vol 47 no 4 pp 271ndash277 2003

[45] A Hatakka ldquoBiodegradation of ligninrdquo in Lignin Humic Sub-stances and Coal M Hofrichter and A Steinbuchel Eds pp129ndash179 Wiley-VCH Weinheim Germany 2001

[46] L-L Kiiskinen K Kruus M Bailey E Ylosmaki M Siika-ahoandM Saloheimo ldquoExpression ofMelanocarpus albomyces lac-case in Trichoderma reesei and characterization of the purifiedenzymerdquoMicrobiology vol 150 no 9 pp 3065ndash3074 2004

[47] G J Mander H Wang E Bodie et al ldquoUse of laccase as anovel versatile reporter system in filamentous fungirdquo Appliedand Environmental Microbiology vol 72 no 7 pp 5020ndash50262006

[48] D A Wood ldquoProduction purification and properties of extra-cellular laccase of Agaricus bisporusrdquo Journal of General Micro-biology vol 117 pp 327ndash338 1980

[49] I Marbach E Harel and A M Mayer ldquoMolecular propertiesof extracellular Botrytis cinerea laccaserdquo Phytochemistry vol 23no 12 pp 2713ndash2717 1984

[50] P Schneider M B Caspersen K Mondorf et al ldquoCharac-terization of a Coprinus cinereus laccaserdquo Enzyme MicrobialTechnology vol 25 pp 502ndash508 1999

[51] M L Niku-Paavola E Karhunen P Salola andV Raunio ldquoLig-ninolytic enzymes of the white-rot fungus Phlebia radiatardquoBiochemical Journal vol 254 no 3 pp 877ndash884 1988

[52] G Sannia P Giardina and M Luna ldquoLaccase from Pleurotusostreatusrdquo Biotechnology Letters vol 8 no 11 pp 797ndash800 1986

[53] J Rogalski T Lundell A Leonowicz and A Hatakka ldquoProduc-tion of laccase lignin peroxidase and manganese-dependentperoxidase by various strains of Trametes versicolor dependingon culture conditionsrdquoActaMicrobiologica Polonica vol 40 pp221ndash234 1991

[54] N T Dittmer R J Suderman H Jiang et al ldquoCharacterizationof cDNAs encoding putative laccase-like multicopper oxidasesand developmental expression in the tobacco hornwormMan-duca sexta and the malaria mosquito Anopheles gambiaerdquoInsect Biochemistry andMolecular Biology vol 34 no 1 pp 29ndash41 2004

[55] Y Taprab T Johjima Y Maeda et al ldquoSymbiotic fungi producelaccases potentially involved in phenol degradation in funguscombs of fungus-growing termites in Thailandrdquo Applied andEnvironmental Microbiology vol 71 no 12 pp 7696ndash77042005

[56] M E Scharf Z J Karl A Sethi and D G Boucias ldquoMultiplelevels of synergistic collaboration in termite lignocellulosedigestionrdquo PLoS ONE vol 6 no 7 Article ID e21709 2011

[57] J Ni and G Tokuda ldquoLignocellulose-degrading enzymesfrom termites and their symbiotic microbiotardquo BiotechnologyAdvances vol 31 pp 838ndash850 2013

[58] M C Monteiro and M E A De Carvalho ldquoPulp bleachingusing laccase from Trametes versacolor under high temperatureand alkaline conditionsrdquo Applied Biochemistry and Biotechnol-ogy Part A vol 70ndash72 pp 983ndash993 1998

[59] T Nishida K Yoshinori A Mimura and Y Takahara ldquoLigninbiodegradation by wood-rotting fungi I Screening of lignin-degrading fungirdquoMokuzai Gakkaishi vol 34 pp 530ndash536 1988

[60] J Luterek L GianfredaMWojtas-Wasilewska et al ldquoScreeningof the wood-rotting fungi for laccase production induction byferulic acid partial purification and immobilization of laccasefrom the high laccase-producing strain Cerrena unicolorrdquo ActaMicrobiologica Polonica vol 46 no 3 pp 297ndash311 1997

[61] J M Harkin and J R Obst ldquoSyringaldazine an effective reagentfor detecting laccase and peroxidase in fungirdquo Experientia vol29 no 4 pp 381ndash387 1973

[62] E De Jong F P de Vries J A Field R P van der Zwan and JA M de Bont ldquoIsolation and screening of basidiomycetes withhigh peroxidative activityrdquo Mycological Research vol 12 pp1098ndash1104 1992

[63] C Raghukumar T M DrsquoSouza R G Thorn and C A ReddyldquoLignin-modifying enzymes of Flavodon flavus a basid-iomycete isolated from a coastal marine environmentrdquo Appliedand Environmental Microbiology vol 65 no 5 pp 2103ndash21111999

[64] M H Gold J K Glenn and M Alic ldquoUse of polymeric dyes inlignin biodegradation assaysrdquoMethods in Enzymology vol 161pp 74ndash78 1988

[65] G Palmieri P Giardina C Bianco B Fontanella andG SannialdquoCopper induction of laccase isoenzymes in the ligninolyticfungus Pleurotus ostreatusrdquo Applied and Environmental Micro-biology vol 66 no 3 pp 920ndash924 2000

[66] R F H Dekker and A M Barbosa ldquoThe effects of aerationand veratryl alcohol on the production of two laccases by theascomycete Botryosphaeria sprdquo Enzyme and Microbial Technol-ogy vol 28 no 1 pp 81ndash88 2001

[67] G Palmieri C Bianco G Cennamo et al ldquoPurificationcharacterization and functional role of a novel extracellularprotease from Pleurotus ostreatusrdquo Applied and EnvironmentalMicrobiology vol 67 no 6 pp 2754ndash2759 2001

[68] J L Dong Y W Zhang R H Zhang W Z Huang and Y ZZhang ldquoInfluence of culture conditions on laccase productionand isozyme patterns in the white-rot fungus Trametes gallicardquoJournal of Basic Microbiology vol 45 no 3 pp 190ndash198 2005

[69] R Gayazov and J Rodakiewicz-Nowak ldquoSemi-continuous pro-duction of laccase by Phlebia radiata in different culturemediardquoFolia Microbiologica vol 41 no 6 pp 480ndash484 1996

[70] R F H Dekker K Y Ling and A M Barbosa ldquoA simplemethod formonitoring chromatography column eluates for lac-case activity during enzyme purificationrdquo Biotechnology Lettersvol 22 no 2 pp 105ndash108 2000

[71] A Piscitelli P Giardina V Lettera C Pezzella G Sannia andV Faraco ldquoInduction and transcriptional regulation of laccasesin fungirdquo Current Genomics vol 12 no 2 pp 104ndash112 2011

[72] E-M Ko Y-E Leem and H T Choi ldquoPurification and charac-terization of laccase isozymes from the white-rot basidiomyceteGanoderma lucidumrdquo Applied Microbiology and Biotechnologyvol 57 no 1-2 pp 98ndash102 2001

[73] C G M De Souza G K Tychanowicz D F De Souza and RM Peralta ldquoProduction of laccase isoforms by Pleurotus pul-monarius in response to presence of phenolic and aromaticcompoundsrdquo Journal of Basic Microbiology vol 44 no 2 pp129ndash136 2004

[74] M Mansur T Suarez J B Fernandez-Larrea M A Brizuelaand A E Gonzalez ldquoIdentification of a laccase gene family inthe new lignin-degrading basidiomycete CECT 20197rdquo Appliedand Environmental Microbiology vol 63 no 7 pp 2637ndash26461997

[75] AM Farnet S Criquet S Tagger G Gil and J Le Petit ldquoPurifi-cation partial characterization and reactivity with aromaticcompounds of two laccases fromMarasmius quercophilus strain17rdquoCanadian Journal ofMicrobiology vol 46 no 3 pp 189ndash1942000

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

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Nucleic AcidsJournal of

Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

16 Enzyme Research

[76] S X Liu J L Dong and Y Z Zhang ldquoAnalysis of laccaseisozymes from Pleurotus osteatusrdquo Sichuan Da Xue Xue Bao(Natural Science Edition) vol 37 pp 769ndash771 2000

[77] P E Courty M Poletto F Duchaussoy M Buee J Garbayeand F Martin ldquoGene transcription in Lactarius quietus-quercuspetraea ectomycorrhizas from a forest soilrdquo Applied and Envi-ronmental Microbiology vol 74 no 21 pp 6598ndash6605 2008

[78] K Brijwani A Rigdon and V Praveen vadlani ldquoFungallaccases production function and applications in food pro-cessingrdquoEnzymeResearch vol 2010Article ID 149748 10 pages2010

[79] G I Zervakis G Venturella and K Papadopoulou ldquoGeneticpolymorphism and taxonomic infrastructure of the Pleurotuseryngii species-complex as determined by RAPD analysisisozyme profiles and ecomorphological charactersrdquo Microbiol-ogy vol 147 no 11 pp 3183ndash3194 2001

[80] E Tanesaka ldquoColonizing success of saprotrophic and ectomy-corrhizal basidiomycetes on islandsrdquoMycologia vol 104 no 2pp 345ndash352 2012

[81] J AMicalesM R Bonde andG L Peterson ldquoIsozyme analysisin fungal taxonomy and molecular geneticsrdquo in Handbook ofApplied Mycology vol 4 of Fungal Biotechnology pp 57ndash791992

[82] K Praveen B Viswanath K Y Usha et al ldquoLignolytic enzymesof a mushroom Stereum ostrea isolated from wood logsrdquoEnzyme Research vol 2011 Article ID 749518 6 pages 2011

[83] M Heinzkill L Bech T Halkier P Schneider and T AnkeldquoCharacterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae)rdquo Applied and EnvironmentalMicrobiology vol 64 no 5 pp 1601ndash1606 1998

[84] A M R B Xavier D V Evtuguin R M P Ferreira and F LAmado ldquoLaccase production for lignin oxidative activityrdquo inProceedings of the 8th International Conference on Biotechnologyin the Pulp and Paper Industry pp 4ndash8 Helsinki Finland June2001

[85] U Kues and M Ruhl ldquoMultiple multi-copper oxidase genefamilies in basidiomycetesmdashwhat forrdquo Current Genomics vol12 no 2 pp 72ndash94 2011

[86] J A Buswell Y Cai and S-T Chang ldquoEffect of nutrientnitrogen and manganese on manganese peroxidase and laccaseproduction by Lentinula (Lentinus) edodesrdquo FEMS Microbiol-ogy Letters vol 128 no 1 pp 81ndash88 1995

[87] A F D Vasconcelos A M Barbosa R F H Dekker IS Scarminio and M I Rezende ldquoOptimization of laccaseproduction by Botryosphaeria sp in the presence of veratrylalcohol by the response-surface methodrdquo Process Biochemistryvol 35 no 10 pp 1131ndash1138 2000

[88] C Srinivasan TMDrsquoSouza K Boominathan andC A ReddyldquoDemonstration of laccase in the white rot basidiomycetePhanerochaete chrysosporium BKM-F1767rdquo Applied and Envi-ronmental Microbiology vol 61 no 12 pp 4274ndash4277 1995

[89] T M DrsquoSouza C S Merritt and C A Reddy ldquoLignin-modi-fying enzymes of the white rot basidiomycete Ganodermalucidumrdquo Applied and Environmental Microbiology vol 65 no12 pp 5307ndash5313 1999

[90] A A S Sinegani G Emtiazia and Hajrasuliha ldquoProductionof laccase by Aspergillus terreus and some basidiomycetes incontaminated media with aromatic compoundsrdquo Asian Journalof Microbiology Biotechnology and Environmental Sciences vol2 pp 1ndash4 2000

[91] R Periasamy and T Palvannan ldquoOptimization of laccaseproduction by Pleurotus ostreatus IMI 395545 using the Taguchi

DOEmethodologyrdquo Journal of BasicMicrobiology vol 50 no 6pp 548ndash556 2010

[92] D S Arora and P K Gill ldquoLaccase production by some whiterot fungi under different nutritional conditionsrdquo BioresourceTechnology vol 73 no 3 pp 283ndash285 2000

[93] A T Thiruchelvam and J A Ramsay ldquoGrowth and laccaseproduction kinetics of Trametes versicolor in a stirred tankreactorrdquo Applied Microbiology and Biotechnology vol 74 no 3pp 547ndash554 2007

[94] V L Papinutti L A Diorio and F Forchiassin ldquoProduction oflaccase and manganese peroxidase by Fomes sclerodermeusgrown on wheat branrdquo Journal of Industrial Microbiology ampBiotechnology vol 30 no 3 pp 157ndash160 2003

[95] P J Strong ldquoImproved laccase production by Trametes pub-escens MB89 in distillery wastewatersrdquo Enzyme Research vol2011 Article ID 379176 8 pages 2011

[96] G Singh N Ahuja M Batish N Capalash and P SharmaldquoBiobleaching of wheat straw-rich soda pulp with alkalophiliclaccase from 120574-proteobacterium JB optimization of processparameters using response surface methodologyrdquo BioresourceTechnology vol 99 no 16 pp 7472ndash7479 2008

[97] M Ye G Li W Q Liang and Y H Liu ldquoMolecular cloning andcharacterization of a novel metagenome-derived multicopperoxidase with alkaline laccase activity and highly soluble expres-sionrdquo Applied Microbiology and Biotechnology vol 87 no 3 pp1023ndash1031 2010

[98] F Zadrazil A Gonser and E Lang ldquoInfluence of incuba-tion temperature on the secretion of extracellular ligninolyticenzymes of Pleurotus sp and Dichomitus squalens into soilrdquo inProceedings of the Conference on Enzymes in the EnvironmentActivity Ecology and Applications pp 12ndash16 Granada SpainJuly1999

[99] A Chernykh N Myasoedova M Kolomytseva et al ldquoLaccaseisoforms with unusual properties from the basidiomycete Stec-cherinum ochraceum strain 1833rdquo Journal of Applied Microbiol-ogy vol 105 no 6 pp 2065ndash2075 2008

[100] K Hilden T K Hakala and T Lundell ldquoThermotolerant andthermostable laccasesrdquo Biotechnology Letters vol 31 no 8 pp1117ndash1128 2009

[101] L Levin F Forchiassin and A M Ramos ldquoCopper inductionof lignin-modifying enzymes in the white-rot fungus TrametestrogiirdquoMycologia vol 94 no 3 pp 377ndash383 2002

[102] P J Collins and A D W Dobson ldquoExtracellular lignin andmanganese peroxidase production by the white-rot fungusCoriolus versicolor 290rdquo Biotechnology Letters vol 17 no 9 pp989ndash992 1995

[103] K Perumal Biochemical studies of lignolytic enzymes of Gon-oderma lucidum a white rot fungus and its application intreatment of paper mill effluent [PhD thesis] University ofMadras Madras India 1997

[104] J R P Cavallazzi C M Kasuya and M A Soares ldquoScreeningof inducers for laccase production by Lentinula edodes in liquidmediumrdquo Brazilian Journal of Microbiology vol 36 no 4 pp383ndash387 2005

[105] D S Arora and P Rampal ldquoLaccase production by somePhlebiaspeciesrdquo Journal of BasicMicrobiology vol 42 pp 295ndash301 2002

[106] T Palvannan and P Sathishkumar ldquoProduction of laccase fromPleurotus floridaNCIM 1243 using Plackett-Burman design andresponse surface methodologyrdquo Journal of Basic Microbiologyvol 50 no 4 pp 325ndash335 2010

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 17

[107] M A A Da Cunha A M Barbosa E C Giese and R F HDekker ldquoThe effect of carbohydrate carbon sources on the pro-duction of constitutive and inducible laccases byBotryosphaeriasprdquo Journal of Basic Microbiology vol 43 no 5 pp 385ndash3922003

[108] D DrsquoSouza-Ticlo A K Verma M Mathew and C Raghuku-mar ldquoEffect of nutrient nitrogen on laccase production itsisozyme pattern and effluent decolorization by the fungusNIOCC2a isolated from mangrove woodrdquo Indian Journal ofMarine Sciences vol 35 no 4 pp 364ndash372 2006

[109] M S Revankar and S S Lele ldquoIncreased production ofextracellular laccase by the white rot fungus Coriolus versicolorMTCC 138rdquo World Journal of Microbiology and Biotechnologyvol 22 no 9 pp 921ndash926 2006

[110] J Sun R-H Peng A-S Xiong et al ldquoSecretory expressionand characterization of a soluble laccase from the Ganodermalucidum strain 7071-9 in Pichia pastorisrdquo Molecular BiologyReports vol 39 pp 3807ndash3814 2012

[111] G F Leatham and T Kent Kirk ldquoRegulation of ligninolyticactivity by nutrient nitrogen in white-rot basidiomycetesrdquoFEMS Microbiology Letters vol 16 no 1 pp 65ndash67 1983

[112] G Janusz J Rogalski M Barwinska and J Szczodrak ldquoEffectsof culture conditions on production of extracellular laccase byRhizoctonia praticolardquoPolish Journal ofMicrobiology vol 55 no4 pp 309ndash319 2006

[113] S Chen D Ma W Ge and J A Buswell ldquoInduction of laccaseactivity in the edible straw mushroom Volvariella volvaceardquoFEMS Microbiology Letters vol 218 no 1 pp 143ndash148 2003

[114] P Baldrian and J Gabriel ldquoCopper and cadmium increaselaccase activity in Pleurotus ostreatusrdquo FEMS MicrobiologyLetters vol 206 no 1 pp 69ndash74 2002

[115] S C Lo Y S Ho and J A Buswell ldquoEffect of phenolic mono-mers on the production of laccases by the edible mushroomPleurotus sajor-caju and partial characterization of a majorlaccase componentrdquoMycologia vol 93 no 3 pp 413ndash421 2002

[116] M E Eugenio J M Carbajo J AMartın A E Gonzalez and JC Villar ldquoLaccase production by Pycnoporus sanguineus underdifferent culture conditionsrdquo Journal of Basic Microbiology vol49 no 5 pp 433ndash440 2009

[117] R K Sharma and D S Arora ldquoProduction of lignocellulolyticenzymes and enhancement of in vitro digestibility duringsolid state fermentation of wheat straw by Phlebia floridensisrdquoBioresource Technology vol 101 no 23 pp 9248ndash9253 2010

[118] J K Gupta S G Hamp J A Buswell and K E ErikssonldquoMetabolism of trans-ferulic acid by the white-rot fungusSporotrichum pulverulentumrdquoArchives of Microbiology vol 128no 4 pp 349ndash354 1981

[119] S B Pointing E B G Jones and L L P Vrijmoed ldquoOpti-mization of laccase production by Pycnoporus sanguineus insubmerged liquid culturerdquoMycologia vol 92 no 1 pp 139ndash1442000

[120] D S Yaver F Xu E J Golightly et al ldquoPurification character-ization molecular cloning and expression of two laccase genesfrom the white rot basidiomycete Trametes villosardquo Applied andEnvironmental Microbiology vol 62 no 3 pp 834ndash841 1996

[121] P J Collins and A D W Dobson ldquoRegulation of laccase genetranscription inTrametes versicolorrdquoApplied andEnvironmentalMicrobiology vol 63 no 9 pp 3444ndash3450 1997

[122] D M Soden and A D W Dobson ldquoDifferential regulation oflaccase gene expression in Pleurotus sajor-cajurdquo Microbiologyvol 147 no 7 pp 1755ndash1763 2001

[123] A Sethuraman D E Akin J G Eisele and K-E L ErikssonldquoEffect of aromatic compounds on growth and ligninolyticenzyme production of two white rot fungi Ceriporiopsis subver-mispora and Cyathus stercoreusrdquo Canadian Journal of Microbi-ology vol 44 no 9 pp 872ndash885 1998

[124] A M Barbosa R F H Dekker and G E St Hardy ldquoVeratrylalcohol as an inducer of laccase by an ascomycete Botryo-sphaeria sp when screened on the polymeric dye Poly R-478rdquoLetters in Applied Microbiology vol 23 no 2 pp 93ndash96 1996

[125] S C Froehner and K E Eriksson ldquoPurification and propertiesof Neurospora crassa laccaserdquo Journal of Bacteriology vol 120no 1 pp 458ndash465 1974

[126] I-Y Lee K-H Jung C-H Lee and Y-H Park ldquoEnhancedproduction of laccase in Trametes vesicolor by the addition ofethanolrdquo Biotechnology Letters vol 21 no 11 pp 965ndash968 1999

[127] S Dhawan andR C Kuhad ldquoEffect of amino acids and vitaminson laccase production by the birdrsquos nest fungus Cyathus bullerirdquoBioresource Technology vol 84 no 1 pp 35ndash38 2002

[128] M T Cambria S Ragusa V Calabrese and A CambrialdquoEnhanced laccase production in white-rot fungus Rigidoporuslignosus by the addition of selected phenolic and aromaticcompoundsrdquo Applied Biochemistry and Biotechnology vol 163no 3 pp 415ndash422 2011

[129] V Elisashvili and E Kachlishvili ldquoPhysiological regulation oflaccase and manganese peroxidase production by white-rotBasidiomycetesrdquo Journal of Biotechnology vol 144 no 1 pp 37ndash42 2009

[130] J A Saraiva A P M Tavares and A M R B Xavier ldquoEffect ofthe inducers veratryl alcohol xylidine and ligninosulphonateson activity and thermal stability and inactivation kinetics oflaccase from Trametes versicolorrdquo Applied Biochemistry andBiotechnology vol 167 no 4 pp 685ndash693 2012

[131] V Elisashvili E Kachlishvili T Khardziani and S N AgathosldquoEVect of aromatic compounds on the production of laccase andmanganese peroxidase by white-rot basidiomycetesrdquo Journal ofIndustrialMicrobiologyampBiotechnology vol 37 no 10 pp 1091ndash1096 2010

[132] T Hadibarata M M Zubir Rubiyatno et al ldquoDegradation andtransformation of anthracene bywhite-rot fungusArmillaria spF022rdquo Folia Microbiologica vol 58 no 5 pp 385ndash391 2013

[133] G M Gadd and L De Rome ldquoBiosorption of copper by fungalmelaninrdquoAppliedMicrobiology and Biotechnology vol 29 no 6pp 610ndash617 1988

[134] S Diwaniyan K K Sharma and R C Kuhad ldquoLaccase from analkali-tolerant basidiomycetesCrinipellis sp RCK-1 productionoptimization by response surfacemethodologyrdquo Journal of BasicMicrobiology vol 52 no 4 pp 397ndash407 2012

[135] C Galhaup and D Haltrich ldquoEnhanced formation of laccaseactivity by the white-rot fungus Trametes pubescens in thepresence of copperrdquo Applied Microbiology and Biotechnologyvol 56 no 1-2 pp 225ndash232 2001

[136] M Huber and K Lerch ldquoThe influence of copper on theinduction of tyrosinase and laccase inNeurospora crassardquo FEBSLetters vol 219 no 2 pp 335ndash338 1987

[137] J K Dittmer N J Patel S W Dhawale and S S DhawaleldquoProduction of multiple laccase isoforms by Phanerochaetechryosporium grown under nutrient sufficiencyrdquo FEMS Micro-biology Letters vol 149 no 1 pp 65ndash70 1997

[138] S Chen W Ge and J A Buswell ldquoBiochemical and molecularcharacterization of a laccase from the edible straw mushroomVolvariella volvaceardquo European Journal of Biochemistry vol 271no 2 pp 318ndash328 2004

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

18 Enzyme Research

[139] Z T Xing J H Cheng Q Tan and Y J Pan ldquoEffect of nut-ritional parameters on laccase production by the culinaryand medicinal mushroom Grifola frondosardquo World Journal ofMicrobiology and Biotechnology vol 22 no 8 pp 799ndash8062006

[140] P Giardina G Palmieri G Cennamo et al ldquoProtein and genestructure of a blue laccase from Pleurotus ostreatusrdquo in Proceed-ings of the 7th International Conference on Biotechnology in thePulp and Paper Industry pp B191ndashB194 Helsinki Finland June1998

[141] Z Liu D Zhang Z Hua J Li G Du and J Chen ldquoA newlyisolated Paecilomyces spWSH-L07 for laccase production iso-lation identification and production enhancement by complexinducementrdquo Journal of Industrial Microbiology amp Biotechnol-ogy vol 36 no 10 pp 1315ndash1321 2009

[142] W Du C Sun J Yu et al ldquoEffect of synergistic inducement onthe production of laccase by a novel Shiraia bambusicola strainGZ11K2rdquo Applied Biochemistry and Biotechnology vol 168 no8 pp 2376ndash2386 2012

[143] AKocyigitM B Pazarbasi I YasaGOzdemir and I KarabozldquoProduction of laccase from Trametes trogii TEM H2 a newlyisolated white-rot fungus by air samplingrdquo Journal of BasicMicrobiology vol 52 pp 661ndash669 2012

[144] S Shankar and S Shikha ldquoLaccase production and enzymaticmodification of lignin by a novel Peniophora sprdquo AppliedBiochemistry and Biotechnology vol 166 no 4 pp 1082ndash10942012

[145] I Robene-Soustrade and B Lung-Escarmant ldquoLaccase isoen-zyme patterns of European Armillaria species from culturefiltrates and infected woody plant tissuesrdquo European Journal ofForest Pathology vol 27 no 2 pp 105ndash114 1997

[146] C Eggert U Temp and K-E L Eriksson ldquoThe ligninolyticsystem of the white rot fungus Pycnoporus cinnabarinuspurification and characterization of the laccaserdquo Applied andEnvironmental Microbiology vol 62 no 4 pp 1151ndash1158 1996

[147] S X F Lu C L Jones andG T Lonergan ldquoCorrelation betweenfungal morphology and laccase expression under the influenceof cellobiose inductionrdquo in Proceedings of the 10th InternationalBiotechnology Symposium and the 9th International Symposiumon Yeasts Sydney Australia 1996 Poster session 1

[148] A M V Garzillo M C Colao C Caruso C Caporale DCelletti and V Buonocore ldquoLaccase from the white-rot fungusTrametes trogiirdquo Applied Microbiology and Biotechnology vol49 no 5 pp 545ndash551 1998

[149] L Gianfreda F Xu and J-M Bollag ldquoLaccases a useful groupof oxidoreductive enzymesrdquo Bioremediation Journal vol 3 no1 pp 1ndash25 1999

[150] IMarbach EHarel andAMMayer ldquoPectin a second inducerfor laccase production by Botrytis cinereardquo Phytochemistry vol24 no 11 pp 2559ndash2561 1985

[151] E Grotewold G E Taccioli G O Aisemberg and N DJudewicz ldquoEarly response and induced tolerance to cyclohex-imide in Neurospora crassardquo Current Genetics vol 15 no 6 pp429ndash434 1989

[152] A Leonowicz and J Trojanowski ldquoInduction of laccase byferulic acid in Basidiomycetesrdquo Acta Biochimica Polonica vol22 no 4 pp 291ndash295 1975

[153] J-M Bollag and A Leonowicz ldquoComparative studies of extra-cellular fungal laccasesrdquo Applied and Environmental Microbiol-ogy vol 48 no 4 pp 849ndash854 1984

[154] M A Pickard R Roman R Tinoco and R Vazquez-DuhaltldquoPolycyclic aromatic hydrocarbon metabolism by white rot

fungi and oxidation by Coriolopsis gallicaUAMH 8260 laccaserdquoApplied and Environmental Microbiology vol 65 no 9 pp3805ndash3809 1999

[155] M Fenice G Giovannozzi Sermanni F Federici and ADrsquoAnnibale ldquoSubmerged and solid-state production of laccaseand Mn-peroxidase by Panus tigrinus on olive mill wastewater-basedmediardquo Journal of Biotechnology vol 100 no 1 pp 77ndash852003

[156] Y Xiao S Zhang Q Hu W Jiang Pu Ch and Y Shi ldquoImmo-bilization of fungal laccase on chitosan and its use in phenoliceffluents treatmentrdquoWeishengwu Xuebao vol 43 pp 245ndash2502003

[157] C G Dosoretz A H-C Chen and H E Grethlein ldquoEffectof oxygenation conditions on submerged cultures of Phane-rochaete chrysosporiumrdquo Applied Microbiology and Biotechnol-ogy vol 34 no 1 pp 131ndash137 1990

[158] N Rothschild Y Hadar and C Dosoretz ldquoLigninolytic systemformation by Phanerochaete chrysosporium in airrdquo Applied andEnvironmental Microbiology vol 61 no 5 pp 1833ndash1838 1995

[159] E N Dombrovskaya and S S Kostyshin ldquoEffects of surfactantsof different ionic nature on the ligninolytic enzyme complexesof the white-rot fungi Pleurotus floridae and Phellinus igniariusrdquoBiochemistry vol 61 no 2 pp 215ndash220 1996

[160] A Lomascolo E Record I Herpoel-Gimbert et al ldquoOver-production of laccase by a monokaryotic strain of Pycnoporuscinnabarinus using ethanol as inducerrdquo Journal of AppliedMicrobiology vol 94 no 4 pp 618ndash624 2003

[161] R Blaich and K Esser ldquoFunction of enzymes in wood destroy-ing fungi II Multiple forms of laccase in white rot fungirdquoArchives of Microbiology vol 103 no 3 pp 271ndash277 1975

[162] P Nandal S R Ravella and R C Kuhad ldquoLaccase productionbyCoriolopsis caperataRCK2011 optimization under solid statefermentation by Taguchi DOEmethodologyrdquo Scientific Reportsvol 3 p 1386 2013

[163] A Jaouani M G Tabka and M J Penninckx ldquoLignin modify-ing enzymes of Coriolopsis polyzona and their role in olive oilmill wastewaters decolourisationrdquo Chemosphere vol 62 no 9pp 1421ndash1430 2006

[164] J C Meza R Auria A Lomascolo J-C Sigoillot and LCasalot ldquoRole of ethanol on growth laccase production andprotease activity in Pycnoporus cinnabarinus ss3rdquo Enzyme andMicrobial Technology vol 41 no 1-2 pp 162ndash168 2007

[165] G Palmieri P Giardina C Bianco A Scaloni A Capassoand G Sannia ldquoA novel white laccase from Pleurotus ostreatusrdquoJournal of Biological Chemistry vol 272 no 50 pp 31301ndash313071997

[166] G Palmieri G Cennamo V Faraco A Amoresano G Sanniaand P Giardina ldquoAtypical laccase isoenzymes from copper sup-plemented Pleurotus ostreatus culturesrdquo Enzyme and MicrobialTechnology vol 33 no 2-3 pp 220ndash230 2003

[167] A-M Farnet S Criquet M Cigna G E Gil and E FerreldquoPurification of a laccase fromMarasmius quercophilus inducedwith ferulic acid reactivity towards natural and xenobioticaromatic compoundsrdquo Enzyme and Microbial Technology vol34 no 6 pp 549ndash554 2004

[168] A-M Farnet S Tagger and J Le Petit ldquoEffects of copperand aromatic inducers on the laccases of the white-rot fungusMarasmius quercophilusrdquo Comptes Rendus de lrsquoAcademie desSciences vol 322 no 6 pp 499ndash503 1999

[169] F Xu W S Shin S H Brown J A Wahleithner U M Sun-daram and E I Solomon ldquoA study of a series of recombinant

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 19

fungal laccases and bilirubin oxidase that exhibit significantdifferences in redox potential substrate specificity and stabilityrdquoBiochimica et Biophysica Acta vol 1292 pp 303ndash311 1996

[170] D S Yaver M D C Overjero F Xu et al ldquoMolecular char-acterization of laccase genes from the basidiomycete Coprinuscinereus and heterologous expression of the laccase Lcc1rdquoApplied and Environmental Microbiology vol 65 no 11 pp4943ndash4948 1999

[171] F Xu ldquoDioxygen reactivity of laccase dependence on laccasesource pH and anion inhibitionrdquo Applied Biochemistry andBiotechnology Part A vol 95 no 2 pp 125ndash133 2001

[172] F Xu ldquoEffects of redox potential and hydroxide inhibition onthe pH activity profile of fungal laccasesrdquo Journal of BiologicalChemistry vol 272 no 2 pp 924ndash928 1997

[173] A M Garzillo M C Colao V Buonocore et al ldquoStructuraland kinetic characterization of native laccases from Pleurotusostreatus Rigidoporus lignosus and Trametes trogiirdquo Journal ofProtein Chemistry vol 20 no 3 pp 191ndash201 2001

[174] B Chefetz Y Chen and Y Hadar ldquoPurification and character-ization of laccase from Chaetomium thermophilium and its rolein humificationrdquo Applied and Environmental Microbiology vol64 no 9 pp 3175ndash3179 1998

[175] H Jung F Xu and K Li ldquoPurification and characterizationof laccase from wood-degrading fungus Trichophyton rubrumLKY-7rdquoEnzyme andMicrobial Technology vol 30 no 2 pp 161ndash168 2002

[176] H Palonen M Saloheimo L Viikari and K Kruus ldquoPurifi-cation characterization and sequence analysis of a laccasefrom the ascomycete Mauginiella sprdquo Enzyme and MicrobialTechnology vol 33 no 6 pp 854ndash862 2003

[177] U A Germann and K Lerch ldquoIsolation and partial nucleotidesequence of the laccase gene from Neurospora crassa aminoacid sequence homology of the protein to human ceruloplas-minrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 83 no 23 pp 8854ndash8858 1986

[178] R Aramayo and W E Timberlake ldquoSequence and molecularstructure of theAspergillus nidulans yA (laccase I) generdquoNucleicAcids Research vol 18 no 11 p 3415 1990

[179] Y Kojima Y Kita and Y Tsukuda ldquoDNA for expression andsecretionrdquo European Patent Application EP0388166 1990

[180] M Saloheimo M-L Niku-Paavola and J K C KnowlesldquoIsolation and structural analysis of the laccase gene from thelignin-degrading fungus Phlebia radiatardquo Journal of GeneralMicrobiology vol 137 no 7 pp 1537ndash1544 1991

[181] C Galhaup S Goller C K Peterbauer J Strauss and D Hal-trich ldquoCharacterization of the major laccase isoenzyme fromTrametes pubescens and regulation of its synthesis by metalionsrdquoMicrobiology vol 148 no 7 pp 2159ndash2169 2002

[182] F Hong N Q Meinander and L J Jonsson ldquoFermentationstrategies for improved heterologous expression of laccase inPichia pastorisrdquo Biotechnology and Bioengineering vol 79 no4 pp 438ndash449 2002

[183] R M Berka S H Brown F Xu P Schneider K M Oxen-boll and D A Aaslyng ldquoPurified Myceliophthora laccasesand nucleic acids encoding samerdquo USA Patent ApplicationUS5981243 1997

[184] E Record P J Punt M Chamkha M Labat C A M J JVan Den Hondel and M Asther ldquoExpression of the Pycnop-orus cinnabarinus laccase gene in Aspergillus niger and char-acterization of the recombinant enzymerdquo European Journal ofBiochemistry vol 269 no 2 pp 602ndash609 2002

[185] D M Soden J OrsquoCallaghan and A D W Dobson ldquoMolecularcloning of a laccase isozyme gene from Pleurotus sajor-caju andexpression in the heterologous Pichia pastoris hostrdquoMicrobiol-ogy vol 148 no 12 pp 4003ndash4014 2002

[186] C Sigoillot E Record V Belle et al ldquoNatural and recombinantfungal laccases for paper pulp bleachingrdquo Applied Microbiologyand Biotechnology vol 64 no 3 pp 346ndash352 2004

[187] M B Kurtz and S P Champe ldquoPurification and characteri-zation of conidial laccase of Aspergillus nidulansrdquo Journal ofBacteriology vol 151 no 3 pp 1338ndash1345 1982

[188] M Paloheimo L Valtakari L Puranen et al ldquoNovel laccaseenzymes and their usesrdquo patent WO2006032724 2006

[189] C Madzak L Otterbein M Chamkha et al ldquoHeterologousproduction of a laccase from the basidiomycete Pycnoporuscinnabarinus in the dimorphic yeast Yarrowia lipolyticardquo FEMSYeast Research vol 5 no 6-7 pp 635ndash646 2005

[190] W Liu Y Chao S Liu H Bao and S Qian ldquoMolecular cloningand characterization of a laccase gene from the basidiomyceteFome lignosus and expression in Pichia pastorisrdquoApplied Micro-biology and Biotechnology vol 63 no 2 pp 174ndash181 2003

[191] P Cassland and L J Jonsson ldquoCharacterization of a gene encod-ing Trametes versicolor laccase A and improved heterologousexpression in Saccharomyces cerevisiae by decreased cultiva-tion temperaturerdquo Applied Microbiology and Biotechnology vol52 no 3 pp 393ndash400 1999

[192] M K Aalto H Ronne and S Keranen ldquoYeast syntaxins Sso1pand Sso2p belong to a family of related membrane proteins thatfunction in vesicular transportrdquoThe EMBO Journal vol 12 no11 pp 4095ndash4104 1993

[193] S Larsson P Cassland and L J Jonsson ldquoDevelopment ofa Saccharomyces cerevisiae strain with enhanced resistance tophenolic fermentation inhibitors in lignocellulose hydrolysatesby heterologous expression of laccaserdquo Applied and Environ-mental Microbiology vol 67 no 3 pp 1163ndash1170 2001

[194] L F Larrondo M Avila L Salas D Cullen and R VicunaldquoHeterologous expression of laccasec DNA from Ceriporiopsissubvermispora yields copper-activated apoprotein and complexisoform patternsrdquo Microbiology vol 149 no 5 pp 1177ndash11822003

[195] A Uldschmid R Dombi and K Marbach ldquoIdentification andfunctional expression of ctaA a P-type ATPase gene involved incopper trafficking in Trametes versicolorrdquoMicrobiology vol 149no 8 pp 2039ndash2048 2003

[196] T Bulter M Alcalde V Sieber P Meinhold C Schlachtbauerand F H Arnold ldquoFunctional expression of a fungal laccasein Saccharomyces cerevisiae by directed evolutionrdquo AppliedEnvironmental Microbiology vol 69 pp 987ndash995 2003

[197] A A Leontievsky T Vares P Lankinen et al ldquoBlue and yellowlaccases of ligninolytic fungirdquo FEMS Microbiology Letters vol156 no 1 pp 9ndash14 1997

[198] G Palmieri P Giardina C Bianco and G Sannia ldquoA novelwhite laccase from Pleurotus ostreatusrdquo in Proceedings of the 7thInternational Conference on Biotechnology in the Pulp and PaperIndustry pp A93ndashA96 Vancouver Canada June 1998

[199] R Bourbonnais and M G Paice ldquoEnzymatic delignification ofkraft pulp using laccase and a mediatorrdquo Tappi Journal vol 79no 6 pp 199ndash204 1996

[200] F S Archibald R Bourbonnais L Jurasek M G Paice and ID Reid ldquoKraft pulp bleaching and delignification by Trametesversicolorrdquo Journal of Biotechnology vol 53 no 2-3 pp 215ndash2361997

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

20 Enzyme Research

[201] R Bourbonnais M G Paice I D Reid P Lanthier and MYaguchi ldquoLignin oxidation by laccase isozymes from Tram-etes versicolor and role of the mediator 221015840-azinobis(3-ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymeriza-tionrdquoApplied and EnvironmentalMicrobiology vol 61 no 5 pp1876ndash1880 1995

[202] R Campos A Kandelbauer K H Robra A Cavaco-Paulo andG M Gubitz ldquoIndigo degradation with purified laccases fromTrametes hirsuta and Sclerotium rolfsiirdquo Journal of Biotechnologyvol 89 no 2-3 pp 131ndash139 2001

[203] T Onuki M Nogucji and J Mitamura ldquoOxidative hair dyecomposition containing laccaserdquo Pat Int Appl WO 0037 030Chemical Abstracts vol 133 p 78994m 2000

[204] P Manzanares S Fajardo and C Martin ldquoProduction ofligninolytic activities when treating paper pulp effluents byTrametes versicolorrdquo Journal of Biotechnology vol 43 no 2 pp125ndash132 1995

[205] C A Reddy and Z Mathew ldquoBioremediation potential ofwhite rot fungirdquo in Fungi in Bioremediation G M Gadd EdCambridge University Press Cambridge UK 2001

[206] M Alexander Biodegradation and Bioremediation AcademicPress San Diego Calif USA 1994

[207] J-M Bollag H-L Chu M A Rao and L Gianfreda ldquoEnzy-matic oxidative transformation of chlorophenolmixturesrdquo Jour-nal of Environmental Quality vol 32 no 1 pp 63ndash69 2003

[208] E Torres I Bustos-Jaimes and S Le Borgne ldquoPotential use ofoxidative enzymes for the detoxification of organic pollutantsrdquoApplied Catalysis B vol 46 no 1 pp 1ndash15 2003

[209] N N Pozdnyakova J Rodakiewicz-Nowak and O VTurkovskaya ldquoCatalytic properties of yellow laccase from Ple-urotus ostreatus D1rdquo Journal of Molecular Catalysis B vol 30no 1 pp 19ndash24 2004

[210] S B Pointing ldquoFeasibility of bioremediation by white-rotfungirdquo Applied Microbiology and Biotechnology vol 57 no 1-2pp 20ndash33 2001

[211] D C Bressler P M Fedorak and M A Pickard ldquoOxidation ofcarbazole N-ethylcarbazole fluorene and dibenzothiopheneby the laccase of Coriolopsis gallicardquo Biotechnology Letters vol22 no 14 pp 1119ndash1125 2000

[212] J Dec and J-M Bollag ldquoPhenoloxidase-mediated interactionsof phenols and anilines with humic materialsrdquo Journal ofEnvironmental Quality vol 29 no 3 pp 665ndash676 2000

[213] M-L Niku-Paavola and L Viikari ldquoEnzymatic oxidation ofalkenesrdquo Journal of Molecular Catalysis B vol 10 no 4 pp 435ndash444 2000

[214] J-M Bollag andCMyers ldquoDetoxification of aquatic and terres-trial sites through binding of pollutants to humic substancesrdquoScience of the Total Environment vol 117-118 pp 357ndash366 1992

[215] M-Y Ahn J Dec J-E Kim and J-M Bollag ldquoTreatmentof 24-dichlorophenol polluted soil with free and immobilizedlaccaserdquo Journal of Environmental Quality vol 31 no 5 pp1509ndash1515 2002

[216] M Gelo-Pujic H-H Kim N G Butlin and G T R PalmoreldquoElectrochemical studies of a truncated laccase produced inPichia pastorisrdquo Applied and Environmental Microbiology vol65 no 12 pp 5515ndash5521 1999

[217] J Riu I Schonsee and D Barcelo ldquoDetermination of sul-fonated azo dyes in groundwater and industrial effluents byautomated solid-phase extraction followed by capillary elec-trophorosismass spectrometryrdquo Journal of Mass Spectrometryvol 33 pp 653ndash663 1998

[218] I M Banat P Nigam D Singh and R Marchant ldquoMicrobialdecolorization of textile-dye-containing effluents a reviewrdquoBioresource Technology vol 58 pp 217ndash227 1996

[219] H Zollinger Synthesis Properties and Applications of OrganicDyes and Pigments Colour chemistry John Wiley-VCH Pub-lishers New York NY USA 2002

[220] V J P Poots G McKay and J J Healy ldquoThe removal of acid dyefrom effluent using natural adsorbents I PeatrdquoWater Researchvol 10 no 12 pp 1061ndash1066 1976

[221] G McKay ldquoWaste color removal from textile effluentsrdquo Ameri-can Dyestuff Reporter vol 68 no 4 pp 29ndash34 1979

[222] H Hou J Zhou J Wang C Du and B Yan ldquoEnhancementof laccase production by Pleurotus ostreatus and its use for thedecolorization of anthraquinone dyerdquo Process Biochemistry vol39 no 11 pp 1415ndash1419 2004

[223] S Rodrıguez Couto M Sanroman and G M Gubitz ldquoInflu-ence of redox mediators and metal ions on synthetic aciddye decolourization by crude laccase from Trametes hirsutardquoChemosphere vol 58 no 4 pp 417ndash422 2005

[224] L Setti S Giuliani G Spinozzi and P G Pifferi ldquoLaccasecatalyzed-oxidative coupling of 3-methyl 2-benzothiazolinonehydrazone and methoxyphenolsrdquo Enzyme and Microbial Tech-nology vol 25 no 3-5 pp 285ndash289 1999

[225] C Raghukumar ldquoFungi frommarine habitats an application inbioremediationrdquoMycological Research vol 104 no 10 pp 1222ndash1226 2000

[226] G M B Soares M Costa-Ferreira and M T Pessoa deAmorim ldquoDecolorization of an anthraquinone-type dye usinga laccase formulationrdquo Bioresource Technology vol 79 no 2 pp171ndash177 2001

[227] G M B Soares M T P De Amorim and M Costa-FerreiraldquoUse of laccase together with redox mediators to decolourizeRemazol Brilliant Blue Rrdquo Journal of Biotechnology vol 89 no2-3 pp 123ndash129 2001

[228] E Abadulla K-H Robra G M Gubitz L M Silva and ACavaco-Paulo ldquoEnzymatic decolorization of textile dyeingeffluentsrdquo Textile Research Journal vol 70 no 5 pp 409ndash4142000

[229] E Rodrıguez M A Pickard and R Vazquez-Duhalt ldquoIndus-trial dye decolorization by laccases from ligninolytic fungirdquoCurrent Microbiology vol 38 no 1 pp 27ndash32 1999

[230] R G Saratale G D Saratale D C Kalyani J S Chang andS P Govindwar ldquoEnhanced decolorization and biodegradationof textile azo dye Scarlet R by using developed microbialconsortium-GRrdquo Bioresource Technology vol 100 no 9 pp2493ndash2500 2009

[231] N Enayatizamir F Tabandeh S Rodrıguez-Couto BYakhchali H A Alikhani and L Mohammadi ldquoBiodegrada-tion pathway and detoxification of the diazo dye Reactive Black5 by Phanerochaete chrysosporiumrdquo Bioresource Technology vol102 no 22 pp 10359ndash10362 2011

[232] R C Miranda E B Gomes N J Pereira M A Marin-Morales K M Machado and N B Gusmao ldquoBiotreatment oftextile effluent in static bioreactor by Curvularia lunata URM6179 and Phanerochaete chrysosporium URM 6181rdquo BioresourceTechnology vol 142 pp 361ndash367 2013

[233] A DrsquoAnnibale S R Stazi V Vinciguerra and G G SermannildquoOxirane-immobilized Lentinula edodes laccase stability andphenolics removal efficiency in olive mill wastewaterrdquo Journalof Biotechnology vol 77 no 2-3 pp 265ndash273 2000

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Enzyme Research 21

[234] G-G Ying B Williams and R Kookana ldquoEnvironmental fateof alkylphenols and alkylphenol ethoxylatesmdasha reviewrdquo Envi-ronment International vol 28 no 3 pp 215ndash226 2002

[235] O P Heemken H Reincke B Stachel and N Theobald ldquoTheoccurrence of xenoestrogens in the Elbe river and the NorthSeardquo Chemosphere vol 45 no 3 pp 245ndash259 2001

[236] J I Lyons S Y Newell A Buchan andM AMoran ldquoDiversityof ascomycete laccase gene sequences in a southeastern US saltmarshrdquoMicrobial Ecology vol 45 no 3 pp 270ndash281 2003

[237] H Bermek K Li and K-E L Eriksson ldquoStudies on mediatorsof manganese peroxidase for bleaching of wood pulpsrdquo Biore-source Technology vol 85 no 3 pp 249ndash252 2002

[238] A M Calvo J L Copa-Patino O Alonso and A E GonzalezldquoStudies of the production and characterization of laccaseactivity in the basidiomycete Coriolopsis gallica an efficientdecolorizer of alkaline effluentsrdquo Archives of Microbiology vol171 no 1 pp 31ndash36 1998

[239] A Taspinar and N Kolankaya ldquoOptimization of enzymaticchlorine removal from Kraft pulprdquo Bulletin of EnvironmentalContamination and Toxicology vol 61 no 1 pp 15ndash21 1998

[240] O Milstein A Haars A Majcherczyk et al ldquoRemoval ofchlorophenols and chlorolignins from bleaching effluent bycombined chemical and biological treatmentrdquo Water Scienceand Technology vol 20 no 1 pp 161ndash170 1988

[241] P Bajpai ldquoApplication of enzymes in the pulp and paperindustryrdquo Biotechnology Progress vol 15 no 2 pp 147ndash157 1999

[242] K K Y Wong J D Richardson and S D Mansfield ldquoEnzy-matic treatment of mechanical pulp fibers for improving paper-making propertiesrdquo Biotechnology Progress vol 16 no 6 pp1025ndash1029 2000

[243] E Abadulla T Tzanov S Costa K-H Robra A Cavaco-Paulo and G M Gubitz ldquoDecolorization and detoxification oftextile dyes with a laccase from Trametes hirsutardquo Applied andEnvironmental Microbiology vol 66 no 8 pp 3357ndash3362 2000

[244] B A Kuznetsov G P Shumakovich O V Koroleva and A IYaropolov ldquoOn applicability of laccase as label in the mediatedand mediatorless electroimmunoassay effect of distance onthe direct electron transfer between laccase and electroderdquoBiosensors and Bioelectronics vol 16 no 1-2 pp 73ndash84 2001

[245] A L Ghindilis V P Gavrilova and A I Yaropolov ldquoLaccase-based biosensor for determination of polyphenols determina-tion of catechols in teardquo Biosensors and Bioelectronics vol 7 no2 pp 127ndash131 1992

[246] R Fogel and J C Limson ldquoElectrochemically predicting pheno-lic substrates suitability for detection by amperometric laccasebiosensorsrdquo Electroanalysis vol 25 pp 1237ndash1246 2013

[247] G T R Palmore and H-H Kim ldquoElectro-enzymatic reductionof dioxygen to water in the cathode compartment of a biofuelcellrdquo Journal of Electroanalytical Chemistry vol 464 no 1 pp110ndash117 1999

[248] GGiovanelli andG Ravasini ldquoApple juice stabilization by com-bined enzyme-membrane filtration processrdquo LWT-Food Scienceand Technology vol 26 no 1 pp 1ndash7 1993

[249] W A Edens T Q Goins D Dooley and J M Henson ldquoPuri-fication and characterization of a secreted laccase of Gaeu-mannomyces graminis var triticirdquo Applied and EnvironmentalMicrobiology vol 65 no 7 pp 3071ndash3074 1999

[250] D Slomczynski J P Nakas and S W Tanenbaum ldquoProductionand characterization of laccase from Botrytis cinerea 61ndash34rdquoApplied and Environmental Microbiology vol 61 no 3 pp 907ndash912 1995

[251] A A Ahmad R Othman F Yusof and M F A Wahab ldquoZinc-laccase biofuel cellrdquo IIUM Engineering Journal vol 12 pp 153ndash160 2011

[252] B Viswanth Laccase from StereumOstrea Production Purifica-tion of Laccase from StereumOstrea LAP LAMBERTAcademicPublishing Saarbrucken Germany 2010

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology