role of mushrooms in soil mycoremediation: a review

http://www.cibj.com/ DOI: 10.19675/j.cnki.1006-687x.2019.04021

Received: 2019-04-09 Accepted: 2019-06-28Supported by the National Natural Science Foundation of China (41571315)Corresponding author (E-mail: [email protected])

Role of mushrooms in soil mycoremediation: a reviewMinhaz Uddin2, Dan Zhang1, Ram Proshad1 & M. K. Haque3

1 Institute of Mountain Hazards and Environment, Chinese Academy of Sciences & Ministry of Water Conservancy, Chengdu 610041, China2 School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, China3 Department of Crop Science and Technology, University of Rajshahi, Rajshahi-6025, Bangladesh

Abstract Bioremediation is an innovative and promising technology available for the removal and recovery of heavy metals from contaminated media. Bioremediation uses organisms to absorb heavy metals at low cost and with no secondary pollution. Bioremediation by macrofungi that degrade pollutants or wastes is referred to as mycoremediation. Macrofungi, like mushrooms, can produce enzymes and have the ability to degrade and accumulate a wide range of toxic metals. In this paper, the research status and advances in the field of mycoremediation using different mushroom species are reviewed. Generally mushrooms use three effective strategies to recover contaminated or polluted soils: biodegradation, bioconversion, and biosorption. Mushrooms can degrade and recycle wastes and pollutants to their mineral constituents and convert wastes, sludge, and pollutants into useful forms. In addition, they can uptake heavy metals from substrates via biosorption, which is a very effective method to reclaim polluted lands. Different wild and cultivated mushroom species are used in mycoremediation, which can degrade large quantities of organic and inorganic pollutants and produce vendible products. Mycoremediation is still in its infancy, but it has notable remediation potential for pollutants or metals in soil. Mushroom species that can biodegrade, bioconvert, or absorb pollutants and metals effectively should be given the highest preference. Further research is needed to verify that this method is an easy, cost effective, and eco-friendly tool.

Keywords bioremediation; mycoremediation; heavy metal; mushroom

Uddin M, Zhang D, Proshad R, Haque MK. Role of mushrooms in soil mycoremediation: a review [J]. Chin J Appl Environ Biol, 2020, 26 (2): 460-468

1 IntroductionMushrooms are available as both wild growing and

cultivated species. These macrofungi have been considered a special food since the earliest times in many countries. Mushrooms can grow everywhere on biological, agricultural, and industrial wastes or can be grown in toxic metal-polluted lands. Mushrooms are considered to be a source of proteins and bio-active molecules with helpful therapeutic applications while being useful in preventing diseases, such as hypertension, hypercholesterolemia [1], and cancer [2]. Mushrooms are very rich in nutritional components, some of which have been compared with animal proteins like those from eggs, milk, and meat [3]. Mushrooms produce single cell proteins, which are easily digestible and more or less free of cholesterol.

Mushrooms are not only an important dietary product, they are also used as a low-cost, effective mycoremediation tool because of their role in the biodegradation, biosorption, and bioconversion of contaminants [4-6]. Mushrooms uptake

and accumulate a considerable amount of heavy metals when they grow on toxic metal-polluted substrates or soil. In addition, mushrooms can accumulate heavy metals from toxic metal-contaminated surfaces [7]. Akin et al. [8] measured the concentrations of Cd, Cr, Cu, Pb, and Zn in Lactarius deliciosus, Russula delica, and Rhizopogon roseolus and obtained mean values of 0.72, 0.26, 28.34, 1.53, and 64 mg/kg, respectively. Furthermore, maximum Cd, Cu, Pb, and Zn concentrations were found in R. delica, while the Cr level was greatest in L. deliciosus. A pot experiment tested the influence of bacterial inoculation on the growth of Coprinus comatus, the content of Ni in C. comatus, Ni speciation in soil, fluoranthene dissipation, soil enzymatic activity, bacterial populations, and community structure. With an inoculation of bacteria, the fresh weight of C. comatus, concentration of Ni in C. comatus, and dissipation rates of fluoranthene increased by 17.73%-29.38%, 68.97%-204.97%, and 34.84%-60.90%, respectively [9].

Zhang Dan et al. [10] studied wild growing mushroom species to investigate the bioaccumulation of heavy metals.

Role of mushrooms in soil mycoremediation: a review 461Vol. 26 No. 2 Apr 2020

They found that Cu, Pb, Cd, and As content in Termitomyces microcarpus were 135.00, 13.28, 65.30, and 1.60 mg/kg, respectively. Agaricus bisporus showed a higher affinity to absorb Cr, Cu, Cd, and Zn. In addition, maximum Zn content was found in Pulveroboletus amarellus and was 142.00 mg/kg in the fruiting body. Several studies for reducing metal concentrations with mushrooms have also been conducted. According to Xu et al., a pot experiment was performed to investigate the combined effects of 2,4,5-trichlorophenol (TCP) and metals on the growth of Clitocybe maxima, and an accumulation of heavy metals as well as the dissipation of TCP were observed [11]. The results showed a negative effect of contamination on the fruiting time and biomass of C. maxima. TCP decreased significantly in soils, accounting for 70.66%-96.24% and 66.47%-91.42% of the initial extractable concentration in planted soil and unplanted soil, respectively, which showed that the dissipation of TCP was enhanced by mushroom planting [11]

.

Zhao et al. developed an effective bottom-up metal removal system, which was based on the synergy between the immobilization of metal-resistant bacteria and the extraction of the bio-accumulator Stropharia rugoso-annulata [12]. The results demonstrated that the system significantly increased the proportion of acid soluble Cd and Cu and improved the soil micro-ecology (i.e., microbial counts, soil respiration, and enzyme activity). The maximum extraction of Cd and Cu was 8.79 mg/kg and 77.92 mg/kg, respectively. In addition, details of the possible mechanisms of metal removal were discussed, and it was found to be positively correlated with acetic acid (HoAc) extractable metals and soil micro-ecology. Meanwhile, the dilution effect in S. rugoso-annulata probably played an important role in the metal removal process [12].

Mushroom mycelia spread over the surfaces where they grow and extract metal ions under suitable conditions. The mycelia extract metals from polluted soil, which leads to a type of mycoremediation known as mycofiltration. Mycelia act like plant roots and extract toxic metals. According to Srivastava et al. [13] and Sesli et al. [2], heavy metal uptake by mushrooms is affected by some environmental factors and the physiology of the mushroom species, such as the pH, metal ion concentration, nature of the fruiting body, age of the mycelia, and the enzymes and proteins present in mushrooms.

The inf luence of chelators and sur factants on the bioaccumulation of heavy metals in the mushroom Tricholoma lobayense Heim from multiple contaminated soi ls was studied. The results showed that a high concentration of EDTA (5 mmol/kg) reduced mushroom biomass by 26%, while the concentrations of Pb, Cu, and Cd in the fruiting bodies increased by 15-88-, 0.8-3.3-, and 0.5-0.6-fold, respectively, when only EDTA was added [14].

2 Remediation through mushroomsMushrooms use three effective methods to reclaim and

ameliorate polluted lands: biodegradation, bioconversion, and biosorption.2.1 Biodegradation

Mushrooms have the ability to accumulate heavy metals with their rich network of hyphae. Each mushroom has a specific capacity and genetically induced ability to absorb heavy metals from the soil [15]. Mushrooms are utilized in mycoremediation because of particular features associated with the potential uptake of heavy metals [16]. Hammel et al. [17] reported that mushrooms have the ability to degrade polycyclic aromatic hydrocarbons (PAHs). The degradation and subsequent recycling of wastes or pollutants by living organisms to their mineral constituents is called biodegradation, while mineralization converts compounds to simple and inorganic forms. A large number of studies have investigated the degradation ability of various mushrooms and their enzymes. Nyanhongo et al. [18] reported that mushrooms can produce extracellular peroxidases, ligninases, cellulases, pectinases, xylanases, and oxidases. Furthermore, mushrooms can degrade PAHs [19], plastic [20], organic and synthetic dyes [21-22], 2,4-dichlorophenol [23], crude oil [24], malachite green [25], and radioactive cellulosic-based waste [26].2.2 Bioconversion

Research on the conversion of wastes, sludge, and pollutants into useful forms is ongoing in many countries. The bioconversion process is based on utilizing sugar from cellulose and hemicellulose to form macrofungi metabolites that are essential for the growth and survival of macrofungi. Wild mushrooms are a potential source of secondary metabolites and enzymes. Secondary metabolites help mushrooms compete and adapt to untoward conditions,

OOOOO

Fig. 1 Primary stages of the degradation process of polycyclic aromatic hydrocarbons (PAHs) by fungi (image modified from Field et al. [27])

26卷第2期 2020年4月 Minhaz Uddin et al.462

and these metabolites are also used for the production of antibiotics, antifungals, nematicides, and vitamins. Macrofungi use enzymes to biodegrade and biotransform the lignin of wood to access cellulose and hemicellulose chains. The enzymes degrade lignocellulosic material into sugar monomers for the production of ethanol by a fermentation process using yeast, which is of industrial interest [28].

Lignocellulosic waste can be used for mushroom cultivation and a bioconversion product can be produced (i.e., a mushroom). Mushroom cultivation in industrial wastes provides protein rich mushroom fruiting bodies and also helps to solve pollution problems. According to Kulshreshtha et al. [29], Pleurotus citrinopileatus successfully grows on industrial waste from handmade paper and produces high quality protein rich fruiting bodies. Jonathan et al. [30] worked with Pleurotus tuber-regium, which grows on trees and produces vendible products. Lentinula edodes is another mushroom species that is able to successfully convert eucalyptus waste to useable products [31]. Two mushroom species, Pleurotus eous and Lentinus conatus, were cultivated by Rani et al. [32] on rice straw and banana waste, and they reported that the rice and banana waste could be bioconverted to usable products. Lechner and Papinutti [33] found that lentinus tigrinus can bioconvert wheat straw. In addition, Volvariella volvacea results in a good production of fruiting bodies when it grows on banana leaves [34]. Gaitán- Hernández et al. [35] cultivated Lentinula edodes and found that this species has the ability to bioconvert barley and wheat straw to maximum yield within 6 days.

Kozarski et al. [36] reported that wild or domestically cultivated macrofungi have the ability to bio-transform vegetal biomass into valuable commercial substances, namely enzymes (e.g., hydrolases and oxidative enzymes), carbohydrates (e.g., β-glucans), proteins (e.g., lectins), and secondary metabolites (e.g., lovastatin). Potential products from macrofungi are also very useful for human activities. For example, enzymes are required in the food, textile,

paper, and pharmaceutical industries. Wild macrofungi supply various enzymes, such as laccase produced by Lactarius sp. [37], Lentinula boryana, and Pycnoporus sp. [38]. In addition, metaloendo-peptidases from Tricholoma saponaceum are able to hydrolyze fibrinogen and fibrin [39].

Trametes versicolor, Irpex lacteus, and Phlebiopsis sp. were found to be useful for lignin degradation with the help of their oxidative activities. This particular ability of these wild strains may be useful for the paper industry [40]. Carbohydrates like β-glucans are used in medicine. Some wild mushrooms, such as Cortinarius violaceus (L. ex Fr.) Gray, Laccaria amethystina (Cooke), Trametes versicolor, and Piptoporus betulinus, produce glucans [41]. Some studies have reported valuable by-products from wild macrofungi, and these are listed in Table 1.2.3 Biosorption

The removal of metals or contaminants by mushrooms f rom an aqueous so lu t ion i s c a l led b iosorp t ion. Gavrilescu [38] reported that biosorption is based on the sorption of metallic ions from effluents by mushrooms with a significant tolerance for metals. Mar’in et al. [48] reported that dead mushroom biomass offers certain advantages over living cell biomass with regard to the biosorption process. Kapoor and Viraraghavan [49] found that the uptake of heavy metals depends on the physico-chemical interactions of metallic ions with the cellular compounds of biological species. Biosorption is a very popular method due to its maximum uptake capacity and low cost. Many mushroom species remove pollutants or heavy metals using biosorption. For example, P. tuber-regium biosorbs heavy metals from heavy metal-contaminated soil [50]. In addition, Fomes fasciatus efficiently biosorps Cu (II) ions, and hot-alkali treatment was found to increase its affinity for Cu (II) ions [51]. Furthermore, Pleurotus platypus, A. bisporus, and Calocybe indica are efficient biosorbents for the removal of Cu, Zn, Fe, Cd, Pb, and Ni from aqueous solutions [6], while Pleurotus ostreatus possesses the biosorption ability to

Fig. 2 Bioconversion pathway to produce by-products with wild mushrooms (image modified from Conceição et al. [28]). (1) Wood is decayed by wild mushrooms, which are natural decomposers. (2) Wild mushrooms bioconvert the nutrients of dead wood into important bioactive molecules. (3) Mushrooms use enzymatic weapons to bioconvert materials. (4) This special arsenal biotransforms plant cell wall components. (5) Cell wall components are biotransformed into oligomers and monomers. (6) Oligomers and monomers undergo a fermentation process. (7) Ethanol and organic acids are produced.


remove cadmium [52], and Pleurotus sajor-caju can biosorb Zn from contaminated sites [53].

Mushrooms or macro fungi can uptake pollutants or heavy metals via bioaccumulation and biosorption processes. Compared to that of plants and vegetables, the fruiting bodies of mushrooms can bioaccumulate large concentrations of heavy metals, as reported by Gast et al. [54]. Mushrooms use mycelium to uptake heavy metals from substrates. The metal content in fruiting bodies is considerably affected by many factors, such as mycelium age, substrate composition, and the life span of fructification. Thomet et al. [55] observed maximum metal concentrations in the sporophores but not the spores, intermediate metal content in the cap, and the lowest

metal content in the stipe. According to Kalac et al. [56], wild grown A. bisporus usually uptake more metals than cultivated Agaricus species. They also added that excess metallic content can be found in mushrooms from ore mining-contaminated sites. The uptake of Cd by Volvariella volvacea and P. sajor-caju can be reduced due to the interaction of Cu and Cd at lower concentrations, but it can increase Cu uptake [57]. However, much is yet to be elucidated of the transport process of metals from mycelium to the fruiting bodies. Previous studies have reported that certain mushrooms have the potential to be biosorbents of metals, and these are presented in Table 2 along with their respective metal concentrations.

Table 1 Bioconversion of vegetal biomass by-productsWild macrofungi Figure Remark Reference

Phlebia sp. This species bioconverts hardwood kraft pulp to ethanol [42]

Cerrena unicolor Cerrena unicolor converts synthetic medium to antioxidant and antimicrobial molecules [43]

Rigidoporus microporus Produce tannin, saponin,alkaloid, steroid, cardiac glycoside [44]

Lactarius sp.Produce laccase

[45]

Coprinus cinereus Cow dungmanure + sisal waste is bioconverted by this species to laccase, lignin peroxidase, and xylanase [46]

Trametes versicolorLaccase, lignin peroxidase, and manganese peroxidase is found from kraft pulp + potato dextrose broth after bioconversion by this species

[40]

Pycnoporuscinnabarinus

Sabouraud dextrose agar is converted to antimicrobial metabolite by this species [47]


3 Barriers to mycoremediation The mycoremediation of polluted lands by mushrooms

is an eco-friendly remediation approach and requires low costs, small areas, and minimally trained personnel. When mycoremediation is carried out in a given site, there is no need to transport the heavy metals to treatment sites, which reduces the transport cost. However, some problems associated with carrying out mycoremediation

are present. Mushrooms need time to remove toxic metals and pollutants from ecosystems and need a considerable amount of time to acclimate. In addition, the toxicity level in the mushrooms themselves is a concern. Toxicity levels in mushrooms increase due to biosorption and biodegradation when they grow on wastes or polluted substrates. Toxicity reduction depends on the ability of mushrooms to degrade wastes or pollutants [71] with their different enzymes. Many

Table 2 Heavy metal uptake capacity of different mushroom species from previous studiesMushroom species Figure Edibility Heavy metal con. in fruiting bodies (mg/kg dry weight) Reference

Agaricus bisporus Edible

Cu 107, Cd 1.7, Pb 2.1, Zn 57.2, Mn 25.9, Fe 290, Cr 6.5, Ni 7.9

Pb 0.46, Cd 0.70, Hg 0.04, Fe 15.8, Cu 6.61, Mn 2.27, Zn 9.32

Pb 2.41, Cd 3.48, Hg 0.60, Cu 5.22,Mn 22.3, Zn 17.8, Fe 126

Cd 3.5

[58]

[59]

[60]

[56]

Armillaria mellea Choice with caution

Pb 1.6, Cd 11.0, Hg 0.3, Cu 31.0

Pb 1.28, Cd 2.48, Hg 0.91, Cu 21.1, Mn 26.8, Zn 76.8

[61]

[62]

Boletus edulis EdiblePb 0.96, Cd 1.03, Hg 0.13, Fe 31.1

Cu 4.7, Mn 2.9, Zn 26.2

[59]

[63]

Calvatia excipuliformis Edible Fe 924, Cu 25, Mn 28, Zn 58, Pb 1.5, Cd 1.1 [8]

Lepiota rhacodes Edible Hg 8, Pb 66, Cd 3.7 [63]

Paxillus involutus Inedible Pb 1.6.0, Cu 57.0 [56, 61]

Pleurotus sajor-caju Edible Pb 7.0 , Cd 33.0 µg/g [45]

Pleurotus ostreatus EdiblePb 0.11, Cd 0.55, Hg 0.31, Fe 48.6, Cu 5.0, Mn 10.3, Zn 19.3；

Pb 3.24, Cd 1.18, Hg 0.42, Fe 86.17，Cu 13.6, Mn 6.2, Zn 29.8

[59]

[62]


studies have reported that mushrooms growing on polluted substrates contain high quantities of metals in their fruiting bodies. Due to the low to intermediate concentrations of heavy metals in substrates, mushroom mycelial growth may be stunted, and higher heavy metal concentrations may inhibit growth. However, some heavy metals are not harmful and can act as growth stimulators (e.g., Zn and Fe). Jain et al. [72] reported that high concentrations of all heavy metals reduced sporocarp production in P. sajor-caju. Purkayastha and Mitra [73] found that Co and Pb caused the highest reduction in the fructification of V. volvacea and P. sajor-caju. In addition, mycelial protein content was reduced in A. bisporus and P. ostreatus due to the uptake of Hg, Cd, Pb, and Zn [74].

4 ConclusionFrom the current review, a great deal of evidence

indicates that mushrooms have effective mechanisms of heavy metal uptake and can degrade different types of wastes, which is very promising for future mycoremediation technologies. Major metal-accumulating, waste-detoxifying,

and pollutant-degrading species have been the focus of mycoremediation research around the globe. However, mycoremediation is still an emerging technology. In my personal view, scientists should first try to cultivate high metal-absorbing mushroom species before low-absorbing mushroom species in waste-containing or polluted sites so that the uptake of the pollutants or metals can be minimized. The toxicity and metal content in mushrooms should be critically assessed so that non-toxic mushrooms may be consumed and health risks avoided. However, in mycoremediation, preference should be given to those species that can biodegrade, bioconver t, or absorb pollutants ef fectively. Fur ther research is needed to support the widespread use of mushrooms as potential mycoremediation tools.

AcknowledgementThe authors would like to thank Dr. Md. Saiful Islam,

Department of Soil Science, Patuakhali Science and Technology University, Bangladesh, for his support and suggestions for this review paper.

Mushroom species Figure Edibility Heavy metal con. in fruiting bodies (mg/kg dry weight) Reference

Psalliota campestris Edible Pb 1.85, Cd 5.55 [64]

Russula delica Edible

Pb 4.8, Cd 2.0, Hg 0.21, Fe 54.5, Cu 10.8, Mn 12.1, Zn 19.3

Cu 73.0, Zn 57.0, Mn 9.6, Fe 244, Co 1.5, Cd 0.31, Ni 3.2, Pb 2.7

Pb 3.1, Cd 1.1, Hg 0.26, Cu 13.6,Mn 6.6, Zn 32.6, Fe 74.8

[59]

[65]

[60]

Coprinus comatus EdiblePb 19.08 ± 2.84, Cu 17.57 ± 0.69, Cd 0.55 ± 0.06

Cu 16.78 × 10-6 Cd 10.83×10-6

[66]

[67]

Lentinus edodes EdibleCr 21.5

Cd 3 mmol/L Fe 3 mmol/L

[68]

[69]

Pleurotus eryngii Edible

Fe 4520.70-3179.15 Zn 98.43-45.92 Cu 95.43-21.70 Mn 37.31-11.46 Ni 28.80-10.90 Pb 25.95-17.38 Cr 18.35-4.25 Co 5.02-1.39

[70]

Table 2 (Continued)


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