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ISSN: 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
Keywords
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
History
Received 12 February 2013
Accepted 27 March 2013
Published online 15 July 2013
20
13
Figure 1. (A) Structure of a typical lignocellulosic residue, (B) Initial fungal attack on
lignin hemicellulose matrix, (C) Degradation
of all three polymers and fungal growth,
(D) Nutritionally upgraded lignocellulose
along with fungal proteins and simple sugars
to be used as animal feed.
(A)
Lignin-Hemicellulose
Matrix
(D)
Hemicellulose
Fungal
proteins
Cellulose
Simple
sugars
Lignin
(C)
DOI: 10.3109/1040841X.2013.791247
Table 1. Comparison of some white rot fungi used for enhancement in digestibility of lignocellulosic residues.
S. No.
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
Ceriporiopsis subvermispora
Cyathus stercoreus
Ganoderma sp.
Candida utilis
Pleurotus ostreatus
Lentinus subnudus
Pleurotus tuber- regim
Pleurotus ostreatus
Trametes versicolor
Pleurotus sajor caju
Pleurotus pulmonarius
Pleurotus florida,
Pleurotus djamor,
Pleurotus sajor-caju
Pleurotus ostreatus
Pleurotus salmoneostramineus
Pleurotus salmoneostramineus
Lentinula edodes
Pleurotus eryngii
Ceriporiopsis subvermispora
Daedalea quercina
Hericium clathroides
Phelinus leavigatus
Inonotus andersnii
Inonotus obliquus
Inonotus dryophilus
Phlebia floridensis
Phlebia radiata
Ceriporiopsis subvermispora
Phlebia brevispora
Phlebia fascicularia
Phanerocheate chrysosporium
Phlebia brevispora
Phlebia fascicularia
Phlebia floridensis
Phlebia radiata
Ceriporiopsis subvermispora
Digestibiltiy
after
degradation
(g/kg)
Enhacement
in digestibility
(%)
Bermuda grass
stems
42
420
527
25
Wheat straw
Apple pomace
305
585
Maize husks
10
6
30
42
Wheat straw
10
299
Maize straw
40
Rice straw
60
423
423
671
Rice straw
Wheat straw
Sugarcane bagasse
50
30
64
Wheat straw
30
655
649
456
456
456
414
Wheat straw
Wheat straw
20
30
175
175
Rice straw
60
185
605
334
633
626
331
288
327
317
511
491
752
696
801
787
791
824
655
460
550
592
563
502
514
520
559
250
232
221
259
231
254
252
237
232
248
240
44
10
8
7
17
1
9
6
21
16
12
4
19
17
21
27
44
1
21
43
36
21
24
26
35
43
33
26
48
32
37
36
28
25
34
30
Lignocellulosic
substrate
% Degradation
Degradation
period (days)
Initial
digestibility
(g/kg)
Symultaneous
Non selective
Selective
Hemicellulose
Cellulose
284
Reference
Akin et al. 1995
Shrivastava et al. 2012
Villas-Boas et al. 2003
Jonathan et al. 2010
Shrivastava et al. 2011
Akinfemi et al. 2009
Mirzaei et al. 2007
DOI: 10.3109/1040841X.2013.791247
Glucose
Cellulose
degradation
(B) Secondary
fungal attack site
H
Hemicellulose
degradation
Lignin
degradation
on
Xylose and
other 5C
sugars
(A) Initial
fungal attack site
Small Phenolics
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), which
assumes 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 degradability (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 nonessential amino acids. However, the essential amino acids
cannot be synthesized and must be provided in the diet.
Nutritionally these amino acids are important because limiting 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 reaction, which can easily be measured colorimetrically.
Ninhydrin method was introduced for quantitative determination 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 instrumental 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
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 functional 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 antioxidants. 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 treatment 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 correlates 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).
DOI: 10.3109/1040841X.2013.791247
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 produced, 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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DOI: 10.3109/1040841X.2013.791247