2013

http://informahealthcare.com/mbyISSN: 1040-841X (print), 1549-7828 (electronic)

Crit Rev Microbiol, Early Online: 19! 2013 Informa Healthcare USA, Inc. DOI: 10.3109/1040841X.2013.791247

REVIEW ARTICLE

Fungal degradation of lignocellulosic residues: An aspect of improvednutritive quality

Rakesh Kumar Sharma1 and Daljit Singh Arora2

1Department of Microbiology, The Maharaja Sayajirao University of Baroda, Vadodara, India and 2Department of Microbiology, Guru Nanak Dev

University, Amritsar, India

Abstract

Microbial degradation of lignocellulosic materials brings a variety of changes in theirbio-physicochemical properties. Lower digestibility of various agricultural residues can beenhanced by microbial treatment. White rot fungi are the potential candidates, which canimprove the nutritional quality of lignocellulosic residues by degrading lignin and convertingcomplex polysaccharides into simple sugars. Changes in physical qualities of lignocellulosicsthat is texture, colour and aroma have been an interesting area of study along with chemicalproperties. Degradation of lignocellulose not only upgrades the quality of degraded biomass,but helps simultaneous production of different commercial enzymes and other by productsof interest. The review is focused on fungal degradation of lignocellulosics, resultant changes inphysicochemical properties and nutritional value.

Keywords

In-vitro digestibility, lignin, lignocellulosedegradation, solid state fermentation,white rot fungi

History

Received 12 February 2013Accepted 27 March 2013Published online 15 July 2013

Introduction

The availability of green fodder is a worldwide problem,

resulting in their scarcity for animal consumption. To

overcome the crisis of feed, several cereal crop residues like

wheat straw (WS), paddy straw (PS), corn stover and so on are

generally used as substitutive fodder and feed supplement.

A variety of food crops are produced around the globe, which

generate enormous agricultural residues. This lignocellulosic

biomass can serve as low cost feed stocks for production

of fuel, ethanol and other value-added commodity chemicals

(Parimala et al., 2007). As compared to forage, cereal straws

are of poor nutritive value and low digestibility because

of their higher lignin content. Lignin is a phenyl-propanoid

biopolymer, resistant to most of the microbial enzymatic

systems and non digestible by ruminants as well. The

presence of lignin and its hemicellulose binding matrix

affects the accessibility of energy rich polysaccharides

(Figure 1).

Degradation of lignin has got the potential to improve

the digestibility of such residues (Arora & Sharma, 2011).

Natural degradation of plant biomass is mainly caused by

different fungal and bacterial species. Holocellulose and

lignin are the biopolymers that are converted into low

molecular weight compounds by the enzymatic action of

these microorganisms (Bugg et al., 2011). Fungi are usually

better degraders of plant cell wall constituents because of

their extracellular enzymatic system and hyphal penetration

power. Many fungal species have been screened for their

potential to degrade various agricultural residues (Wan & Li,

2011). White rot fungi degrade lignin efficiently and select-

ively by using their ligninolytic enzyme system which mainly

comprises of laccase, lignin peroxidase and manganese

peroxidase, along with many other enzymes (Arora et al.,

2002; Arora & Sharma, 2010).

Fungal ligninolysis and break down of cellulose-hemi-

cellulose matrix liberate simple degradable components that

can be easily utilized by rumen microflora, thus improving

the ruminant digestibility. Bioconversion of these residues

into more nutritive animal feed has fascinated many workers

to work on the problem and make it practically possible at

lab-level fermentation (Bisaria et al., 1997; Chalamcherla

et al., 2009). Solid state fermentation (SSF) of agroresidues

is an advantageous method to degrade lignin and improve

their digestibility. Fungi grown under these conditions

not only cause better ligninolysis but also improve digestibil-

ity by enhancing the accessibility of holocellulose (Okano

et al., 2006).

White rot fungi are well known producers of lignocellu-

lolytic enzymes including lignin modifying enzymes, hemi-

cellulases and cellulases. Degradation of holocellulose along

with lignin results into higher loss in total organic matter

(TOM), which limits the practical use of such agro residues as

feed. The degradation of useful holocellulose can be

minimized by using selective ligninolytic fungi (Tuyen

et al., 2012). Phanerocheate chrysosporium is a well known

white rot fungus and widely studied for lignin degradation

(Syed & Yadav, 2012). However, loss of TOM is very high

during the degradation of lignocellulosics, which necessitates

the need to look for selective ligninolytic organisms

Address for correspondence: Daljit Singh Arora, Ph D, Department ofMicrobiology, Guru Nanak Dev University, Amritsar, 143005 India.E-mail: daljit_02@yahoo.co.in

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(Jung et al., 1992). Selective lignin degrading organisms

possess the potential capability for improvement of digestibil-

ity of agro-residues (Arora & Gill, 2000; Vares et al., 1994).

Quality of straw depends upon the composition of its

cell wall fibers, that is neutral detergent fiber (NDF), acid

detergent fiber (ADF), water solubles, hemicellulose, cellu-

lose, lignin, protein and ash content, where higher ADF value

and lignin content results in less digestibility (Garcia et al.,

2003). Digestibility measured by in-vitro methods gives a

close idea about the quality of feed (Goering & Van Soest,

1970). An increase in dry matter digestibility shows increased

quality of feed and less feed intake. Some physical properties

of straw, e.g. swelling capacity, moisture content, pH, etc. also

affect the digestibility and feed quality. Protein and amino

acid content of the feed are also important factors regulating

its nutritive value. Thus, different compositional analyses of

sound and delignified straw are done to know their nutritive

quality (Shrivastava et al., 2012).

In the present status report, keeping in mind the poor

nutritive quality of agricultural residues and dismal scenario

of green feed for ruminants, the fungal degradation of agro-

residues using some selective ligninolytic fungi and measures

of nutritive quality along with the biochemical changes in

agroresidues is discussed. The importance of SSF as an eco-

friendly system to convert abundantly available agricultural

residues in to nutritive animal feed is also being highlighted.

Evaluation of nutritional quality

According to Alves De Brito et al. (2003), evaluation of the

nutritional quality of forage requires the detailed analysis

of the composition of its cell wall. The digestibility of cell

wall is influenced by both, the contents and physical

characteristics of wall polysaccharides such as degree of

crystallinity and polymerization (Fritz et al., 1990).

Role of chemical constituents in digestibilityof plant cell wall

Composition and constituents of cell wall play an important

role to determine the digestibility. Richness in holocellulosic

components enhances the digestibility. However, lignin plays

a major role in protecting the substrate from microbial and

chemical attacks as this is the most resistant part in plant cell

wall. The high level of lignification and silicification limits

ruminal degradation of the carbohydrates and the low content

of nitrogen are the main deficiencies of rice straw, affecting

its value as feed for ruminants (Van Soest, 2006).

Ash constitutes the inorganic matter mainly containing

minerals and is also difficult for animal digestion but required

in trace amounts. As ash does not contain any energy, so it

would naturally lower the overall energy and digestibility of

the feed (Fonnesbeck et al., 1981). Minerals also act as barrier

against the attack of rumen microbes to structural carbohy-

drates. The physical barrier concept is best described by

making use of the rumen as the rumen being an anaerobic

environment, it is clear that access and attachment of the

microorganism to the substrate is vital if efficient cellu-

lose hydrolysis is to be effected (Malherbe & Cloete,

2002). Fungal delignification increases the surface area of

lignocellulosics, thus providing better opportunity to the

rumen microorganisms which not only enhances the digest-

ibility of the feed but also improves their nutritional value

(Figure 1).

In-vitro digestibility (IVD)

Digestibility measured by in-vitro methods gives a close idea

about the quality of feed (Goering & Van Soest, 1970), as this

provides a quick and precise prediction of in-vivo digestibility

in ruminants. The in-vitro procedure does a better job of

Figure 1. (A) Structure of a typical lignocel-lulosic residue, (B) Initial fungal attack onlignin hemicellulose matrix, (C) Degradationof all three polymers and fungal growth,(D) Nutritionally upgraded lignocellulosealong with fungal proteins and simple sugarsto be used as animal feed.

Fungal proteins

Simple sugars

Lignin

Hemicellulose

Cellulose

Lignin-Hemicellulose Matrix

Initial fungal attack site

(A)

(B) (C)

(D)2 R. K. Sharma & D. S. Arora Crit Rev Microbiol, Early Online: 19

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prediction than chemical composition because it accounts

for all factors affecting digestibility, whether known or

unknown, which is not possible by present chemical methods

(Garcia et al., 2003).

The two stage in-vitro procedure developed by Tilley &

Terry (1963) is the most reliable laboratory method for

predicting the digestibility of a wide range of forages. It can

predict in-vivo digestibility with a lower error than any

chemical method and has been widely accepted throughout

the world for measuring the digestibility of feeds (Minson,

1990; Shrivastava et al., 2012). Many fungi produce cellulase,

hemicellulase and other enzymes that degrade forage carbo-

hydrates. Jones and Hayward (1973) showed that a commer-

cially available fungal cellulase could be used to predict

forage digestibility with an accuracy similar to that achieved

with the method of Tilley & Terry. Unfortunately, these

cellulase preparations are relatively expensive and not readily

available in less developed countries. Consequently, enzym-

atic methods have generally received less attention than the

procedure of Tilley & Terry.

The first stage of the Tilley & Terry (1963), technique

simulates conditions in the reticulorumen and requires an

inoculum of rumen microorganisms obtained from sheep or

cattle fitted with a rumen fistula. The use of fistulated animals

for this purpose has been criticized on ethical grounds, and

there are also many practical reasons for reducing the need

for fistulated animals in nutritional studies including (a) It

requires special surgical skills, (b) fistulated animals need

special care to ensure that the fistula is kept free of any

infection and (c) a uniform diet must be fed if the inoculum

is to have constant activity. These conditions are often

difficult or impossible to achieve in the humid tropics and

in less-developed countries (Akhter et al., 1999). It is also

difficult to handle an animal for practical use in a typical

microbiology lab.

One method of overcoming the need for rumen- fistulated

animals is to use freshly voided faeces from sheep as the

source of inoculum (El Shaer et al., 1987). Akhter et al (1999)

concluded that bovine faeces have the potential as an

alternative to rumen liquor from rumen-fistulated sheep

when estimating digestibility using the in-vitro technique.

Further, the method involving the use of enzymes like

cellulase is relatively expensive, while the one using feacal

inoculum for determining the digestibility is comparatively

cheaper and easy laboratory method and equally effective as

that of using rumen fluid (Arora & Sharma, 2009a, 2011;

Dhanoa et al., 2004; Utomo et al., 2011).

Correlation between lignin content and in-vitrodigestibility

Cell wall constituents of straw play an important role in

determining its quality as animal feed. Lignin being a

phenolic biopolymer seems to be difficult to be digested by

ruminants. Higher lignin and tannin content results into lower

digestibility of lignocellulosics and plant residues (Arigbede

et al., 2012). As evident from earlier observations, a strong

negative correlation existed between lignin content and

in-vitro digestibility of undecayed paddy straw samples,

while a strong positive correlation was observed between

lignin loss and in-vitro digestibility of degraded straw (Arora

& Sharma, 2009b; Sharma & Arora, 2011a). As also reported

by Cohen et al. (2002) that during selective lignin degrad-

ation, the cellulose is exposed and can be utilized by

ruminants. It strengthens the viewpoint that delignification

plays an important role in improvement of the digestibility

and feed value of straw. Several workers have been

demonstrated successful bioconversion of lignocellulosic

residues into nutritive animal feed using white rot fungi

under solid state degradation (Table 1).

Degradation of lignocellulosic residues andin-vitro digestibility

On the basis of lignin degradation, ligninolytic fungi can be

classified into three categories (a) simultaneous, (b) non-

selective and (c) selective lignin degrading fungi (Figure 2).

White rot fungi are known to attack initially on the

hemicellulose lignin matrix (Martnez et al., 2005) using

xylanase, esterase and other ligninolytic enzymes; the esterase

cleaves covalent bonds between polysaccharides and lignin

(Dong et al., 2013). Phlebia spp. degraded higher amount of

lignin selectively during SSF of lignocellulose without much

loss in cellulose (Arora & Sharma, 2009a; Sharma & Arora,

2010a). Fast growing white rot fungi P. chrysosporium grow

vigorously and degrade hemicellulose and cellulose much

faster than lignin in paddy straw while during wheat straw

(WS) degradation almost equal amount of these fibres were

degraded, while more lignin was degraded during sugarcane

baggases as compared to other fibers (Sharma & Arora,

2010b; Dong et al., 2013).

Several white rot fungi have been evaluated for their

potential to degrade lignocellulosics and their resultant effect

on digestibility. Well studied white rot fungus P. chrysospor-

ium, non selective in lignin degradation degrades all the fibres

simultaneously which results in more holocellulose loss and

thus degraded a large amount of TOM (Chang et al., 2012).

On the other hand, Phlebia spp. degrade much lower TOM

during the fermentation process, which accounts for more

selective ligninolysis leaving behind a sufficient amount

of TOM. Thus, a reasonable amount of easily digestible

degraded biomass is available to the animal as feed (Sharma

& Arora, 2010a). For practical purposes, higher loss in TOM

severely limits the use of P. chrysosporium (Jung et al., 1992).

The degradation profile of P. chrysosporium indicates that the

higher holocellulose degradation may be due to the higher

production of polysaccharide degrading enzymes (Kerem

et al., 1992; Deshpande et al., 2009).

Cellulase and hemicellulase like enzymes break down

the complex polysaccharides into simple sugars, which

contribute to major part of water solubles. The water soluble

part provides easily digestible components which can be

used by rumen microflora and contributes to the digestibility

of straw. No direct correlation could be established between

the water soluble content, fiber degradation and digestibility

(Rolz et al., 1986). It may also be possible that the fungi

use the easily available sugars for their own growth also

(Nigam et al., 2009), which thus lead to underestima-

tions of soluble components and may interfere with the

interpretations.

DOI: 10.3109/1040841X.2013.791247 Fungal degradation of lignocellulosic residues 3

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In a study on paddy straw degradation, no significant

enhancement in the in-vitro digestibility could be achieved

during initial days of straw fermentation. However, the

digestibility increases during the later period of incubation

(Sharma & Arora, 2011b) suggesting that, initially the fungi

need some easily available components for their own growth

thus limiting the availability of simple sugars for rumen

microflora. As observed by Dorado et al. (1999), composition

of the water soluble fraction correlated with the extent of

straw transformation. The initial fermentation stage (015

days) was characterized by the accumulation of water-soluble

products from straw degradation and fungal metabolism, the

concentration of which tended to stabilize in the later

stage (1660 days). In most of the cases, the water soluble

components were not liberated at a constant rate during fungal

degradation, while the fiber degradation and digestibility

increased steadily. It suggests that digestibility also depends

upon the availability of other polysaccharides as well as the

structure of polymers (Bertrand et al., 2006) that are modified

by the fungal enzymatic treatment.

Hemicelluloselignin matrix is primarily attacked by

white rot fungi moath; relatively higher amounts of lignin

Table 1. Comparison of some white rot fungi used for enhancement in digestibility of lignocellulosic residues.

S. No. White rot fungiLignocellulosic

substrateDegradationperiod (days)

Initialdigestibility

(g/kg)

Digestibiltiyafter

degradation(g/kg)

Enhacementin digestibility

(%) Reference

1 Ceriporiopsis subvermispora Bermuda grassstems

42 420 527 25 Akin et al. 1995

2 Cyathus stercoreus 605 443 Ganoderma sp. Wheat straw 10 305 334 10 Shrivastava et al. 20124 Candida utilis Apple pomace 6 585 633 8 Villas-Boas et al. 20035 Pleurotus ostreatus 30 626 76 Lentinus subnudus Maize husks 42 284 331 17 Jonathan et al. 20107 Pleurotus tuber- regim 288 18 Pleurotus ostreatus Wheat straw 10 299 327 9 Shrivastava et al. 20119 Trametes versicolor 317 6

10 Pleurotus sajor caju Maize straw 40 423 511 21 Akinfemi et al. 200911 Pleurotus pulmonarius 423 491 1612 Pleurotus florida, Rice straw 60 671 752 12 Mirzaei et al. 200713 Pleurotus djamor, 696 414 Pleurotus sajor-caju 801 1915 Pleurotus ostreatus 787 1716 Pleurotus salmoneostramineus Rice straw 50 655 791 21 Miki & Okano 200517 Pleurotus salmoneostramineus Wheat straw 30 649 824 2718 Lentinula edodes Sugarcane bagasse 64 456 655 44 Okano et al. 200619 Pleurotus eryngii 456 460 120 Ceriporiopsis subvermispora 456 550 2121 Daedalea quercina Wheat straw 30 414 592 43 Jalc et al. 199722 Hericium clathroides 563 3623 Phelinus leavigatus 502 2124 Inonotus andersnii 514 2425 Inonotus obliquus 520 2626 Inonotus dryophilus 559 3527 Phlebia floridensis Wheat straw 20 175 250 43 Arora & Sharma 2009b28 Phlebia radiata Wheat straw 30 175 232 33 Arora & Sharma 2009a29 Ceriporiopsis subvermispora 221 2630 Phlebia brevispora 259 4831 Phlebia fascicularia 231 3232 Phanerocheate chrysosporium Rice straw 60 185 254 37 Sharma & Arora 2010a33 Phlebia brevispora 252 3634 Phlebia fascicularia 237 2835 Phlebia floridensis 232 2536 Phlebia radiata 248 3437 Ceriporiopsis subvermispora 240 30

Symultaneous Non selective Selective

Types of lignin degradation

Lignin Hemicellulose Cellulose

% D

egra

datio

n

Figure 2. Simultaneous lignin degradation (degradation of all threepolymers occurs with almost same rate and upto a similar quantity);non-selective lignin degradation (degradation of lignin is lesser thanholocellulose); Selective lignin degradation (degradation of lignin ishigher than holocellulose).

4 R. K. Sharma & D. S. Arora Crit Rev Microbiol, Early Online: 19

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and hemicellulose degradation as compared to cellulose.

During an earlier study (Xu et al., 2010) on corn stover

degradation by Irpex lacteus, lignin and hemicellulose were

also selectively degraded over cellulose. Degradation of

lignin and hemicellulose was correlated in a strong positive

manner (Arora & Sharma, 2009b; Tuyen et al., 2012). Even

under varied nutritional environment, lignin hemicellulose

matrix were attacked initially, indeed the rate and efficiency

of the degradation being different (Arora and Sharma, 2011;

Sharma & Arora, 2010b). Thus, hemicellulose degradation

and in-vitro digestibility may also be positively correlated

(Agosin et al., 1985). Hemicellulose and lignin showed

the largest proportionate degradation in WS after incubation

with the D. quercina, H. clathroides, P. laevigatus, and

L. obliquus, while the other fungi caused the maximum loss

in cellulose and hemicellulose contents. It suggests that the

digestion enhancement of wheat straw colonized by white

rot fungi is regulated by complex factors including the

degradation of structural carbohydrates and lignin (Jalc et al.,

1998). Figure 3 shows initial and secondary fungal attack

sites and the release of simple monomer units from the

complex polymers.

Selective ligninolysis may be characterized by a higher

positive correlation between TOM loss and lignin loss as

compared to the polysaccharide degradation. Lignin must

be a major component of degraded TOM in comparison

to hemicellulose and cellulose (Chang et al., 2012).

Ligninolysis, loss in TOM and IVD of PS is illustrated in

Figure 1. The lignin loss was relatively lesser as compared to

the loss in TOM during PS degradation by P. chrysosporium,

while in all other cases it was relatively higher than TOM loss

and clearly reflected selectivity towards lignin degradation by

all Phlebia spp (Sharma & Arora, 2010a).

Crude protein

Feed protein content is generally expressed in the form of

crude protein. Crude protein is termed crude because it is not

a direct measurement of protein but is an estimation of total

protein based on nitrogen (N 6.25 crude protein), whichassumes 16 g of N/100 g of protein in feeds. Crude protein

includes true protein and non-protein nitrogen (NPN) such as

urea nitrogen and ammonia nitrogen. The crude protein value

provides no information about amino acid composition,

intestinal digestibility of the protein, or its rumen degrad-

ability (Garcia et al., 2003; Rotz, 2004). Generally, growth of

fungal mycelium increases total protein content of the feed

(Fazaeli, 2007). Fungal degradation of straw enhanced

crude protein content (Sharma & Arora, 2010a) and in vivo

N intake by the animal (Shrivastava et al., 2012). Selection of

selective lignin degrading fungi over the cellulose and their

capability of synthesizing proteins with high nutritional

value are necessary during SSF of lignocellulosics (Zhu

et al., 2011).

Amino acids

Proteins are composed of amino acids, which are required for

the maintenance, growth, and productivity of animals. A total

of about 22 amino acids have even identified of which the

animal can synthesize about half; which are called non-

essential amino acids. However, the essential amino acids

cannot be synthesized and must be provided in the diet.

Nutritionally these amino acids are important because limit-

ing these will affect the growth and development of the

animal. Supplemental amino acids can be added to feedstuff

to increase efficiency of animal production and achieve a low

cost feed formulation. Analyzing the amino acid composition

of feedstuffs ensures that nutritionists provide a more precise

feed formulation (Rotz, 2004). SSF of lignocellulosics also

improves the available amino acid content of the residual

biomass (Chalamcherla et al., 2010; Arora & Sharma, 2011).

It is important to measure the amino acid content during

lignocellulosic degradation to be used as feed.

To measure the amino acid content during lignocellulosic

degradation to be used as feed, an instant and reliable method

is needed to analyze the samples. Amino acids produce the

typical purple-blue or yellow colour during ninhydrin reac-

tion, which can easily be measured colorimetrically.

Ninhydrin method was introduced for quantitative determin-

ation of amino acids in the late 1940s. The method was

originally developed for chromatographic elution from amino

acid analyzer (Moore & Stein, 1948), this method has also

been adapted for determination of amino group containing

compounds in foods as well as various types of samples

(Hurst et al., 1995; Panasiuk et al., 1998). Although instru-

mental methods such as amino acid analyzer and HPLC are

currently used for determining compounds containing amino

group, the simple and convenient ninhydrin method still

possess several advantages because no expensive equipment

is required, and it is suitable for the routine analysis of large

numbers of samples. The method has also been used for the

quantitative analysis of amino acids in a variety of agricultural

residues (Friedman, 2004). The modifications suggested

by Sun et al. (2006) make ninhydrin method even more

Lignin degradation

Hemicellulose degradation

Cellulose degradation

on

H

(A) Initial fungal attack site

(B) Secondary fungal attack site

Glucose

Xylose and other 5C sugars

Small Phenolics

Figure 3. Degradation of lignocellulose by selective ligninolyticfungi; (A) Initially, ligninases and hemicellulases trigger the degrad-ation of lignocellulose; (B) cellulose degradation starts along withhemicellulose.

DOI: 10.3109/1040841X.2013.791247 Fungal degradation of lignocellulosic residues 5

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convenient, less expensive, and less time consuming for

quantification of compounds containing amino group.

Antioxidants

Vitamin E, vitamin C, carotenoids, and some trace minerals

are important antioxidant components of animal feed and

their role in animal health and immune function are

indispensable (Roeder, 1995). Free radicals are mainly

reactive oxygen species (ROS) and reactive nitrogen species

(RNS) and include not only the oxygen or nitrogen radicals,

but some non-radical reactive derivatives of oxygen and

nitrogen. These free radicals are constantly produced during

normal physiological metabolism in tissues and damage the

biologically important molecules such as DNA, proteins,

lipids, and carbohydrates (Bellomo, 1991). Under normal

conditions the deleterious effects of ROS/RNS are countered

by the bodys antioxidant defenses, which are contributed

through dietary intake of key nutrients (e.g. vitamins and trace

minerals). Antioxidants serve to stabilize these highly reactive

free radicals, thereby maintaining the structural and func-

tional integrity of cells. Thus, along with nutritive feed the

antioxidants are very important for the immune system and

health of the animals (Chew, 1995; Weiss, 2005).

A variety of polyphenols contributes to the antioxidant

potential of feed (Gladine et al., 2007). Cereal straw contains

lignin, which are complex phenolic polymers and exhibit a

very poor solubility. This may limit their reactivity with the

radicals responsible for the oxidation and subsequently limit

their protective effect compared to that of synthetic antioxi-

dants. As reported by Pan et al. (2006), the lignin with more

phenolic hydroxyl groups, less aliphatic hydroxyl groups, low

molecular weight, and narrow polydispersity showed high

antioxidant activity. The delignification involve the cleavage

of covalent linkages of the lignin, which results into the

formation of low-molecular weight units holding a great value

in antioxidant enhancement (Pouteau et al., 2003). Thus,

degradation of lignin enhances smaller phenolic units and

holds the potential to upgrade the quality of lignocellulosic

residue by enhancing its antioxidant property. Fungal treat-

ment of tomato pomace and some agricultural residues to

upgrade the low-quality feed into antioxidants rich nutritional

feed (Assi & King, 2007; Lateef et al., 2008). Total phenolic

content (TPC) and antioxidant activity of WS and PS

significantly increased during fungal degradation. TPC cor-

relates positively with antioxidant activities; indicating the

bioactive potential of phenolic compounds, which neutralize

the free radicals (Arora et al., 2011). Thus, ligninolysis of

lignocellulosic residues provides an added feature to the feed

by enhancing its antioxidant potential (Pouteau et al., 2003;

Sharma et al., 2010).

Fungal degradation of lignocellulosic residues andassociated changes in physicochemical properties

Fungal degradation of straw brings about a variety of changes

in the biological, chemical, and physical properties of the

substrates, that is change in colour, aroma, pH, and enhance-

ment in total phenolic content. These changes may be because

of the production of intermediate compounds formed during

fungal degradation of lignin, cellulose, or hemicellulose.

Visual observation showed the change in texture (increased

degree of roughness) and colour (turned pinkish-white) during

degradation process, which might be due to (1) breakdown of

complex plant cell wall polymers, (2) fungal growth on the

substrate, and (3) simultaneous production of some metabol-

ites/by products. Commission Internationale de leclairage

(CIE) colour measurements used for the colorimetric analysis

of degraded lignocellulose showed that yellow and red colour

was significantly higher in degraded straw (Arora et al.,

2011). This change in colour might be contributed by the

quinone like smaller phenolic compounds, which are reported

to be coloured in general and yellow or brown in specific

(Murata et al., 2002).

The change in pH may be the result of the production

of acidic compounds by the degradation of complex sugar

and lignin. A decline in pH was recorded during fungal

degradation different lignocellulosics (Dong et al., 2013).

Studies have reported the formation of a mixture of acids

including aromatic carboxylic acids during lignin degradation

e.g. benzoic acid, p-methoxybenzoic acid, veratrum acid,

i-hemipinic acid, Phenoxyacetic acid, 2-methoxyphenylacetic

acid, salycylic acid, trans-cinnamic acid and so on along with

some -keto acids, which are converted to aromatic carboxylic

acids in a second oxidation step with hydrogen peroxide

(Javor et al., 2003; Ko et al., 2009). Various pathways

describing the bacterial and fungal degradation of lignin

and its by products were well discussed during earlier review

(Bugg et al., 2011).

Similarly, the change in aroma that is having slightly

pungent smell of degraded straw indicates the presence of

aldehydes and/or acidic compounds. Several compounds

including carboxylic, aldehydes, and ketone groups were

identified as intermediate or by products before the complete

mineralization of the lignin (Maman et al., 1996). The

metabolic pathway of the fungi plays an important role in the

production of different intermediate compounds, which

depends upon their enzymatic activity, fungal strain, and

substrate. Some fungi efficiently mineralize lignin in a short

period while others take longer time and produce higher

amount of smaller/monomer phenolic units (Tuomela et al.,

2002). The studies have shown not so uniform increase in

the TPC produced, which did not show a similar rate of

enhancement as the degradation of lignin. This can be

attributed to either complete degradation of lignin to CO2 and

H2O, while in some fungi high TPC associated with low

lignin loss indicate the production of smaller phenolic units

and their further degradation to a limited extent. A positive

correlation between TPC and lignin loss showed the enhance-

ment in smaller phenolic units during the break down of

lignin (Arora et al., 2011). The slight difference in TPC and

lignin degradation may be due to the difference in the pattern

of ligninolysis, quality, and quantity of smaller phenolic units

formed, their solubility and further transformation as well

(Yang et al., 2010).

Ash constitutes inorganic matter and is required in trace

amounts. As ash does not contain any energy, so it would

naturally lower the overall energy of the feed (Fonnesbeck

et al., 1981; Frei et al., 2011). During fungal degradation of

lignocellulosic residues the ash content seems to be increased

(Akinfemi et al., 2009). Ash content of the degraded straw

6 R. K. Sharma & D. S. Arora Crit Rev Microbiol, Early Online: 19

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varies depending upon the other constituents of straw as

well as the fungal species used for the degradation. The rate

and efficiency of degradation also affect the ash content

in the residual biomass. In general, organism capable of

degrading higher amount of lignocellulose leaves a higher

amount of residual ash. The lignocellulose degraded by

P. chrysosporium contains a large amount of ash (22 %),

while in the straw degraded by P. brevispora had a lower

ash content (12.6 %). This positive correlation between ash

content and TOM loss, indicates that the residual ash

constituents were not utilized by the fungi; thus the fungus

causing maximum TOM also contributes in higher ash

content. Thus, the higher ash content in degraded straw may

be a factor for its lower IVD even after degrading sufficient

amount of lignin (Sharma & Arora, 2010a). Both of these

factors (enormous loss of lignocellulosic resides and

increased ash content) must be kept in mind while choosing

the fungus to be used for processing of lignocellulosic

residues for animal feed production. In contrast, the ash

content showed a weak positive correlation with in-vitro

digestibility.

Toxicity of fermented animal feed

Different workers have used white rot fungi to upgrade the

nutritive quality of lignocellulosic residues. Apparently, no

case has been reported for the pathogenicity of these fungi

towards human and animal species. The potential for

biological hazard is low for the microbially converted feeds

so far evaluated (Banerjee et al., 2000; Sinskey & Batt, 1987).

During a recent study on fungal fermented wheat straw

(Sharma et al., 2012), different mycotoxins (aflatoxins) were

observed but the levels of the toxins in all the diets were far

below to the permissible levels (20 ppb) in the feeds meant

for immature animals (Food and Drug Administration, USA

(USFDA)) and poultry (Bureau of Indian Standards (BIS)).

Nevertheless, this hazard has to be continually evaluated by

various biological studies when a new microbial fermented

product is proposed.

Mycotoxins are secondary metabolites produced by fungal

species mainly including Aspergillus, Penicillium, Fusarium,

Alternaria, and Stachybotrys spp. During the growth of the

moulds on food and feed stuff the toxins may be produced.

A number of bioassays using cell culture techniques have

been described for the toxicological characterization of

mycotoxins. A colorimetric cell culture assay using 3-(4,5-

dimethylthiazolyl-2)-2,5 diphenyltetrazolium bromide (MTT)

is an important measure of cellular toxicity, firstly used by

Mosmann (1983). MTT can reflect the sensitivity of live cells

to extrinsic stimulation; therefore, it also has an important

value to assess cell viability. Earlier, to detect toxin effects in

in-vitro cell models, the (MTT) dye reduction assay has been

shown to be an effective indicator of fungal toxicity (Gilbert

& Slavik, 2004; Maenetje et al., 2008).

Some mycotoxins especially Aflatoxin B1 was reported

to be highly mutagenic in the Salmonella typhimurium

(Ames test) system (Ciegler & Bennett, 1980). Ames test

is well known for the assessment of mutagenic activity.

Feed extract against S. typhimurium was used to evaluate the

mutagenic activity of extract (Arora et al., 2011).

As reported by Zadrazil (2000), some fungi decompose

lignin and other substrate components, but in-vitro digestibil-

ity decreases. This may be due to toxicity for the rumen

microorganisms of substrate extracts that are used for the

determination of in-vitro digestibility. This concept is also

helpful to know about the toxicity of fermented feed towards

rumen microflora. Tests for toxicity of the organism and the

treated biomass as well as large scale setup along with animal

trials are necessary to further evaluate the potential of solid

state fungal treatment of lignocellulose (Akin et al., 1993).

Conclusions

Looking for a solution to the problem related to scarcity

of green fodder and simultaneously managing lignocellulosic

wastes seems to be a fastidious approach. A positive

correlation between ligninolysis and digestibility gives an

idea for the removal of lignin using selective lignin degrading

white rot fungi. During the degradation of complex

lignocellulosics various intermediate by products are pro-

duced, which affect the physicochemical and nutritional

quality of degraded residues. Increase in nutritive value

during fungal degradation can be summarized in following

steps (a) break down of lignin-polysaccharide binding matrix,

(b) reduction in lignin content, (c) increased surface area for

the better access of energy containing fibers, (d) conversion of

complex polysaccharides into simple sugars, (e) increased

protein content and antioxidants. The points discussed, may

be useful for analytical aspect of microbiologically treated

feed stuff.

Declaration of interest

The authors report no conflict of interest. The authors alone

are responsible for the content and writing of this article.

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