Appl Microbiol Biotechnol (2012) 96:863–873
DOI 10.1007/s00253-012-4446-9
MINI-REVIEW
Potential uses of spent mushroom substrate and its associated
lignocellulosic enzymes
Chia-Wei Phan & Vikineswary Sabaratnam
Received: 1 August 2012 / Revised: 14 September 2012 / Accepted: 17 September 2012 / Published online: 30 September 2012
# Springer-Verlag Berlin Heidelberg 2012
Abstract Mushroom industries generate a virtually in-
exhaustible supply of a co-product called spent mushroom
substrate (SMS). This is the unutilised substrate and the
mushroom mycelium left after harvesting of mushrooms.
As the mushroom industry is steadily growing, the volume
of SMS generated annually is increasing. In recent years, the
mushroom industry has faced challenges in storing and
disposing the SMS. The obvious solution is to explore new
applications of SMS. There has been considerable discussion
recently about the potentials of using SMS for production of
value-added products. One of them is production of lignocel-
lulosic enzymes such as laccase, xylanase, lignin peroxidase,
cellulase and hemicellulase. This paper reviews scientific
research and practical applications of SMS as a readily avail-
able and cheap source of enzymes for bioremediation, animal
feed and energy feedstock.
Keywords Spent mushroom substrate . Spent mushroom
compost . Lignocellulosic enzyme . Bioremediation .
Animal feed . Energy feedstock
Introduction
The ever-increasing human demand for protein-rich food
and the inefficiency of conventional methods have resulted
in the need to explore alternatives for low cost production of
unconventional protein-rich food (Mukherjee and Nandi
C.-W. Phan : V. Sabaratnam (*)
Mushroom Research Centre, Institute of Biological Sciences,
Faculty of Science, University of Malaya,
50603 Kuala Lumpur, Malaysia
e-mail: viki@um.edu.my
C.-W. Phan
e-mail: phanchiawei@gmail.com
2004). One of the options is edible fungi or mushrooms
belonging to the Basidiomycetes. To date, the mushroom
industry is an industry with world production greater than
25 mt. The current largest mushroom producer of mush-
rooms, China has attained more than 20 mt and accounted
for over 80 % of the world's mushroom production (Li
2012). Correspondingly, production of 1 kg of mushrooms
will generate 5 kg of spent residual material called spent
mushroom substrate (SMS) (Lau et al. 2003). An average
farm discards about 24 t of SMS per month (Singh et al.
2011). In Ireland, approximately 254,000 t of SMS is gen-
erated each year (Barry et al. 2012) and in The Netherlands,
more than 800,000 t of SMS is produced per year (Oei and
Albert 2012). In some countries, waste management of SMS
is a major problem faced by farmers. Apparently, the obvious
solution is to increase the demand for SMS through explora-
tion of new applications for utilisation. It would be more
economical and favourable if SMS is to be recycled and re-
used. Considering the high organic matter of SMS, rapid
advances have been made and the number of scientific re-
search has increased in the past few years. This work presents
a state of the art review on SMS with emphasis on recent
advances in enzyme production for bioremediation, animal
feeding and potential usage in alternative energy.
Mushroom production
Worldwide, the top three mushroom species cultivated are
the white button mushroom (Agaricus bisporus), shiitake
(Lentinula edodes) and oyster mushroom (Pleurotus spp.)
(Suguimoto et al. 2001; Li 2012). Cultivation of these
mushrooms represents a major industry in the countries of
Southeast Asia (Chang and Miles 1989; Mehta et al. 1990;
Ragunathan and Swaminathan 2003). Amongst the different
cultivated species, genus Pleurotus is important industrially,
864
occupying a third place in worldwide production of edible
mushrooms, i.e., 16.3 % of the total production (Chang
1996). Pleurotus spp. can grow and produce fruit bodies in
temperate and tropical zones and does not require any pre-
treatment of substrate. The production of Pleurotus spp.
results in a large amount of protein (as extra-cellular enzymes)
on substrates consisting primarily of agro-industrial and for-
estry waste materials (Poppe 2000). In Malaysia, Pleurotus
spp. are the major cultivated mushrooms and account for 90 %
of the local production compared to other species such as L.
edodes and Auricularia polytricha (Saidu et al. 2011). The
Peoples' Republic of China is the major producer and con-
sumer of Pleurotus spp., accounting for nearly 90 % of the
total world production (Royse et al. 2004). In South Korea, the
area of mushroom cultivation has increased to 1,102 km2 and
117,600 t of mushroom was produced in 2000 (Ko et al.
2005). It has been reported that approximately 600 t of
SMS is produced in South Korea annually, of which
58 % is from Pleurotus ostreatus cultivation. In the
United States, the annual production of Pleurotus spp. has
reached 880 t in 1996 and it has increased by 120-fold in 2002
(Royse et al. 2004). In 2010/2011, the oyster mushroom
production has exceeded 3,700 tonnes in the United States
(United States Department of Agriculture 2012). In Ireland,
mushroom production is an appreciable industry and has been
estimated to contribute approximately £90 million to the
economies of both Northern Ireland and the Republic of
Ireland (Russell et al. 2005; Williams et al. 2001). In Northern
Ireland, 24,000 t of mushrooms are produced annually, offer-
ing 3,000 jobs to the nation.
The fate of spent mushroom substrate
SMS is a composted organic medium that results from the
mushroom cultivating process. The term “spent mushroom
compost” (SMC) is used interchangeably with “spent mush-
room substrate” (SMS) describing the agro-residues and
fungal mycelium left after harvesting of mushrooms. SMS
is commonly made from renewable agricultural residues
such as sawdust, sugarcane bagasse, oil palm empty fruit
bunch, wheat straw-bedded horse manure, hay, poultry ma-
nure, ground corncobs, cottonseed meal, cocoa shells, gyp-
sum and other substances (Jordan et al. 2008). Generally,
each cultivation cycle lasts for 5 to 6 months and the spent
substrate will be disposed (Fig. 1). In Malaysia, an average
farm producing 100 t of fresh mushrooms per annum gen-
erated approximately 438 t of SMS. The current disposal
strategy of SMS in Malaysia is by burning, spreading on
land, burying, composting with animal manure, or landfill-
ing. One of the main difficulties in the management of SMS
is the lack of waste management supervision (Magette et al.
1998) and the other obstacles are summarised in Table 1.
Appl Microbiol Biotechnol (2012) 96:863–873
Enzyme recovery
Mushroom enzymes reported in the literature are derived from
mycelia of macro-fungi grown in submerged fermentation.
Enzymes can also be extracted from solid substrate fermenta-
tion technology which is a process mimicking nature (Pandey
et al. 2000). In Malaysia, lignocellulosic agricultural residues
like sago hampas, oil palm frond parenchyma tissue and
rubber wood sawdust are abundant and readily available
(Annuar et al. 2010; Kumaran et al. 1997). These “woody”
biomaterials which mainly consist of fibre, when supple-
mented with rice bran and calcium carbonate, are excellent
sources of substrates to cultivate mushrooms. After harvesting,
the spent mushroom compost will have plenty of extra-cellular
enzymes. Of all the enzymes, laccase (EC 1.10.3.2) is the most
reserved and common in SMS from A. bisporus (Mayolo-
Deloisa et al. 2009), Pleurotus sajor-caju (Kumaran et al.
1997; Singh et al. 2003), P. ostreatus, L. edodes, Flammulina
velutipes and Hericium erinaceum (Ko et al. 2005). However,
lignin peroxidase productivity (per microgram of SMS) was
found to be the highest from the SMS of P. sajor-caju (Singh
et al. 2003) and it was two-, 22-, 30-, 86-fold higher than that
of β-glucosidase, laccase, xylanase and cellulase, respectively.
It is believed that the type of enzymes produced by mushroom
during cultivation is directly affected by the ingredient of
growing substrates and the species of mushrooms (Ball and
Jackson 1995). Table 2 summarises the types of enzymes
detected and extracted from SMS of selected mushrooms.
Another important aspect on enzyme recovery from SMS
is the optimisation of the extraction methods. Certain meth-
ods for extraction and purification of enzymes, for example,
laccase have been reported, including dialysis, ultra-
filtration, anion-exchange chromatography and gel filtration
(Chen et al. 2004; Nagai et al. 2002; Quaratino et al. 2007;
Ullrich et al. 2005), However, most of the investigations
were carried out using fruiting body or mycelium of mush-
room, not the SMS. Potential use of aqueous two-phase
systems (Benavides and Rito-Palomares 2008) is also gain-
ing interest and this method resulted in “one-single primary
recovery stage” that gave a 95 % yield of laccase recovery
(Mayolo-Deloisa et al. 2009). To sum up, the important
parameters are pH, temperature, extraction medium, incuba-
tion time, inocula density and nitrogen source.
Application of SMS and the associated lignocellulosic
enzymes
Bioremediation
Mushrooms are ligninolytic fungi and represent an important
organism in natural recycling events and in bioremediation
(Gadd 2001). The enzyme systems of mushrooms contain
Appl Microbiol Biotechnol (2012) 96:863–873 865

Fig. 1 The mushroom production cycle from preparation of mushroom substrate to disposal

lignin peroxidase, laccase and manganese-dependent peroxi-
dase (Table 3) which catalyses metabolisation of many lignin-
like structures, for example, PAHs and phenols. Bioremedia-
tion by means of immobilised enzymes extracted from the
fruiting bodies and mycelia of mushrooms are appealing.
However, only in this decade, greater attention has been
drawn to reuse SMS and the enzymes recovered from it as
an economical approach in bioremediation of such pollutants
(Eggen and Sasek 2002).
Polycyclic aromatic hydrocarbons
Polycyclic aromatic hydrocarbons (PAHs) belong to a class
of organic compounds that are persistent and recalcitrant in
the environment. Biodegradation of PAHs especially by
white-rot fungus Pycnoporus sanguineus is considered en-
vironmentally friendly when compared to the conventional
physical–chemical remediation which might lead to second-
ary contamination and the need for additional post-treatment
(Annuar et al. 2009). Vikineswary et al. (2006) have shown
that a higher laccase productivity (7.60 U/g substrate) dur-
ing solid substrate fermentation of sago hampas was
achieved as compared to oil palm frond parenchyma tissue
(7.52 U/g substrate) and sawdust (5.68 U/g). The capacity of
P. sanguineus to remove PAHs like anthracene, phenan-
threne and pyrene was attributed to the enzyme laccase
secreted (Munusamy et al. 2008). The immobilised P. san-
guineus laccase, however, exceeded the efficiency of the

Table 1 Obstacles in SMS management as reviewed by Magette et al. (1998)

Obstacles in SMS management Description Solution to overcome

Unsupervised SMS management
Plastic mushrooms bags
Incineration
Burning
Shortage of land and landfill sites
Contractors have been given the full authority to dispose SMS,Possible license apply directly to SMS
most often by using unsustainable disposal practices waste from government authority
Non-biodegradable plastic bags from the SMS ended up A proper plastic recycling strategy needs
co-disposed in landfills to be established
Not economically practical and received no public supports Exploration of new utilisation of SMS
Not environmental friendly, emission of smoke and fine 1. Enzyme recovery
particulate matter PM10 2. Bioremediation
Lands are very competitive for use by extensive mushroom 3.Animal feed
producers. The levels of N and P of SMS to be spread must be 4. Energy feedstock
controlled
5. Crop production
866 Appl Microbiol Biotechnol (2012) 96:863–873

Table 2 Different lignocellulosic enzymes detected in SMS of mushrooms

Enzyme Mushroom Component of SMS Reference

α-Amylase EC 3.2.1.1 Pleurotus ostreatus Sawdust Ko et al. (2005)

Cellulase EC 3.2.1.4
β-Glucosidase EC 3.2.1.21 Lentinula edodes
Laccase EC 1.10.3.2 Flammulina velutipes
Xylanase EC 3.2.1.8 Hericium erinaceum
Lignin peroxidase EC 1.11.1.14 Pleurotus sajor-caju Sawdust; sago hampas Kumaran et al. (1997)
Cellulase EC 3.2.1.4 from sago palm Singh et al. (2003)
β-Glucosidase EC 3.2.1.21 (Metroxylon sagu)
Laccase EC 1.10.3.2
Xylanase EC 3.2.1.8
Xylan-degrading enzymes Endoxylanase Commercial SMS Wheat straw Ball and Jackson (1995)
6-Xylosidase
Arabinofuranosidase
Acetylesterase
Cellulose-degrading enzymes Endoglucanase
Cellobiosidase
β-Glucosidase
Lignin-degrading enzymes Peroxidase
Phenol oxidase
Laccase EC 1.10.3.2 Agaricus bisporus – Mayolo-Deloisa et al. (2009)

free mycelia culture when the fungus was immobilised on
Ecomat, which is made from oil palm empty fruit bunch mat
(Low et al. 2008; Low et al. 2009).
Now, the potential of SMS in bioremediation of PAH
has attracted more attention. Bioremediation by employ-
ing crude extracts containing PAH-degrading enzymes
from SMS are supposed to be more economical com-
pared to pure enzyme/s. Purification of pure enzyme is
often expensive and has limited application in bioreme-
diation. However, it could not be a one-to-one relation-
ship between PAH degradation rate and a particular
enzyme activity, since crude extracts contained more
than one enzyme. An intergraded waste management
approach by combining ozone oxidation pre-treatment
and SMS-mediated aerobic biological treatment of
benzo(α)pyrene was granted successful (Russo et al.
2012). The matrix of Pleurotus pulmonarius-degraded
paddy straw consist predominantly –OH groups which
hypothetically contributed by the cellulosic cell wall of
plant matter and they facilitated the biosorption of PAHs
(Lau et al. 2003). Laccase was found in the SMS of P.
pulmonarius and its activity was 1.5-fold higher than
that of manganese peroxidase (MnP). Interestingly, no
ligninase was found. By applying 5 % (w/w) of P. pulmonar-
ius SMS, the degradative removal efficiencies of naphthalene,
phenanthrene, benzo[a]pyrene and benzo[g; h; i]perylene was
100 % and the degraded products were less toxic compared to
the original pollutants (Lau et al. 2003). More recently, pilot-
scale PAH removal capacity of P. ostreatus SMS in Nigerian
oil-based drill cuttings has been investigated and after 56 days,
the degradation of total PAHs was as high as 92.38 %
(Ayotamuno et al. 2010).
Besides that, the highest total degradation rate of 15
PAHs were achieved by adding crude extracts from Pleuro-
tus eryngii SMS, followed by A. bisporus, P. ostreatus and
Coprinus comatus (Li et al. 2010). Interestingly, laccase
activity from the crude extracts of SMS from P. eryngii
was not the highest amongst all. This showed that the lac-
case activity was not positively correlated to the PAH deg-
radation rate, implying that natural mediators present in
different crude extracts might contribute to the degradation
rate, rather than laccase alone. Eggen (1999) also found that
there was no positive correlation between laccase activity
and PAH degradation rate.
Phenolic compounds
Phenol and polyphenolic compounds are toxic pollutants
and represent a major organic component in some industrial
wastewaters. Oxidation of phenol by crude extracts of SMS
from A. bisporus was reported and laccase was identified
as the main enzyme responsible for the oxidation (Trejo-
Hernandez et al. 2001). The findings of Hublik and Schinner
(2000) also supported the idea of de-contaminating phenolic
compounds using edible mushroom SMS as a source of
crude laccase.
Appl Microbiol Biotechnol (2012) 96:863–873 867

Table 3 SMS for the bioreme-

diation of different types of
pollutants
Type of pollutant
Polycyclic aromatic hydrocarbons
Phenolic compounds
Biocide and fungicide
Petroleum
Heavy metal
Synthetic and textile dye
Acid mine drainage
Type of SMS
Agaricus bisporus
Pleurotus eryngii
Pleurotus ostreatus
Coprinus comatus
Pleurotus pulmonarius
Pleurotus ostreatus
Agaricus bisporus
Pleurotus pulmonarius
Agaricus bisporus
Agaricus bisporus (75 %) and
Pleurotus sp. (25 %)
Agaricus blazei
Pleurotus pulmonarius
Lentinula edodes
Pleurotus sajor-caju
Pycnoporus sanguineus
Lentinus polychrous
Pleurotus ostreatus
Not determined
Reference
Li et al. (2010)
Lau et al. (2003)
Eggen (1999)
Ayotamuno et al. (2010)
Trejo-Hernandez et al. (2001)
Chiu et al. (1998)
Law et al. (2003)
Córdova Juarez et al. (2011)
Ahlawat et al. (2010)
Karanasios et al. (2010)
Kadian et al. (2008)
Gonzalez Matute et al. (2012)
Chiu et al. (2009)
Chen et al. (2005)
Singh et al. (2002)
Singh et al. (2010)
Annuar et al. (2009)
Khammuang and Sarnthima (2007)
Papinutti and Forchiassin (2010)
Zhou et al. (2011)
Cheong et al. (2010)
Newcombe and Brennan (2010)

Biocide and fungicide
Pentachlorophenol (PCP) is a wide-spectrum pesticide and
its toxicity against many organisms has rendered biodeg-
radation from being used. Chiu et al. (1998) were proba-
bly one of the first who reported that the SMS of P.
pulmonarius performed better than various mushroom my-
celia, namely, Armillaria gallica, Armillaria mellea,
Ganoderma lucidum, L. edodes, Phanerochaete chryso-
sporium, P. pulmonarius, Polyporus sp., Coprinus ciner-
eus and Volvariella volvacea, in decontamination of PCP.
Similarly, a high biodegradation capacity, i.e., 15.5 ±
1.0 mg of PCP by 1 g of SMS from P. pulmonarius
was reported (Law et al. 2003). The removal process
was mainly contributed to by the immobilised enzymes
secreted by the mushroom during production and also the
biosorption of PCP by chitin (Chiu et al. 1998; Law et al.
2003). Further, SMS of A. bisporus and its dominating
microbes were found to be able to biodegrade agricultural
fungicides, namely, carbendazim and mancozeb, both in
vitro and in situ (Ahlawat et al. 2010). The indigenous
fungi and bacteria associated to the SMS of A. bisporus
were Trichoderma sp. and Aspergillus sp; B-1 and B-IV
bacterial isolates, respectively. It was the extra-cellular
lignolytic enzymes in SMS that helped in fungicide deg-
radation. However, the enzymes were not identified. In
Mexico, enzyme laccase, MnP and phenol oxidase were
detected in a crude extract of SMS from P. pulmonarius
(Córdova Juarez et al. 2011). Accordingly, chlorothalonil,
a broad-spectrum organochlorine fungicide, at the initial
concentration of 2 mg/l, could be 100 % degraded by a
freshly prepared SMS extract from P. pulmonarius. More
recently, the crude enzyme derived from SMS of Agaricus
blazei was demonstrated to degrade metsulfuron methyl, a
sulfonylurea herbicide, with no or low phytotoxicity to-
wards oil rape (Brassica napus L.) (Gonzalez Matute et
al. 2012). Collectively, these findings open the possibility
of reusing SMS from mushroom industries for degrading
herbicides and pesticides which have harmful eco-
toxicological effects.
The concept of using SMS as a soil amendment in bio-
stimulation was also appealing. Generally, biostimulation is
868
the improvement of the intrinsic degradation potential of a
polluted environment upon introduction of amending
agents. SMS is a good candidate of a biostimulation agent
as it harvests many enzymes. In a study by Kadian et al.
(2008), the dissipation rate of atrazine which is a kind of
restricted-use herbicide was enhanced by a commercial
SMS at 29.17 %, representing a 1.3-fold better performance
by using farmyard manure. In the La Rioja region of Spain,
the effect of addition of SMS from A. bisporus (75 %) and
Pleurotus sp. (25 %) was tested as a soil amendment on the
fate of a copper-based fungicide to a vineyard soil. The
results showed that the increase in organic matter due to
the application of SMS did not engender any significant
retention or persistence of copper in the soil over time
(Herrero-Hernández et al. 2011). In Southern Europe, SMS
from A. bisporus was tested along with four other agricul-
tural composts as biomixture components in a biobed sys-
tem to minimise point source contamination of water
resources by pesticides. The degradation and adsorption
rates of a mixture of pesticides, namely, dimethoate, indox-
acarb, buprofezin, terbuthylazine, metribuzin, metalaxyl-M,
iprodione and azoxystrobin, were significantly higher than
those of the corresponding controls (Karanasios et al. 2010).
Total petroleum hydrocarbon
SMS of P. pulmonarius was used to treat petroleum, oil and
grease, and di(2-ethylhexyl) phthalate (DEHP)-contaminat-
ed soil and the results were very promising (Chiu et al.
2009). The removal mechanism included first the
hydrocarbon-degrading enzymes that SMS possessed, i.e.,
laccase (1.0–1.5 Umg−1) and MnP (0.8–0.9 Umg−1). Sec-
ondly, SMS harboured a rich amount of native microbes,
i.e., bacteria of (11±3)×107 cfug−1 and fungi of (56±9)×
104 cfug−1 for bio-augmentation. Finally, the treatment com-
petency was explained partially by the macro- and micro-
nutrients in SMS that modulate the microbial community.
Moreover, the high soil moisture, relatively low bulk density
and high porosity of SMS provide a favourable environment
for biodegradation (Chiu et al. 2009; Molina-Barahona et al.
2004; Rivera-Espinoza and Dendooven 2004).
Heavy metal
Although the removal of heavy metal by SMS reported by
Chen et al. (2005) is not caused directly by enzymatic
reaction but by the biomass component, it is worthy to
discuss the use of SMS (L. edodes in this case) as a novel
biosorbent for heavy metals like cadmium, lead and chro-
mium. Cellulose is the main biomass component in SMS of
L. edodes (22.86 %, g/g), followed by hemicellulose
(19.71 %) and lignin (10.24 %). A scanning electron micro-
scope and Fourier transform infrared spectrometry revealed
Appl Microbiol Biotechnol (2012) 96:863–873
that at least three functional groups, i.e., carboxyl, phospho-
ryl and phenolic groups, on these polymers served as the
biding sites for heavy metals. The maximum uptake (qm) of
Cd (II) estimated using the Langmuir sorption model was
833.33 mg/g which was 56-, 16.9- and fivefold higher when
compared to that of chitin, Schizomeris leibleini and Tra-
metes versicolor. The maximum uptake of Pb (II) was
1,000.00 mg/g, which was also considered much higher than
other fungi. However, Cr (III) uptake by SMS was moderate
(44.44 mg/g) when compared to brown seaweed biomass
(34.10 mg/g) and brown seaweed Sargassum wightii
(81.70 mg/g). As a conclusion, SMS could be an efficient
biosorbent of heavy metals for decontamination of polluted sites.
Dye decolourisation
SMS of P. sajor-caju offer an economical advantage of
obtaining industrially important enzymes like lignin perox-
idase, laccase, β-glucosidase, carboxymethyl cellulose and
xylanase to decolourise dyes (Singh et al. 2002). Laccase of
Lentinus polychrous was found to be effective in decolou-
rising dye like remazol brilliant blue R (Khammuang and
Sarnthima 2007). With reference to Singh et al. (2010), eight
dyes (tryphan blue, amido black, remazol brilliant blue R,
bromophenol blue, crystal violet, methyl green, congo red
and methylene blue) were decolourised by lignin peroxidase
extracted from 5-month-old SMS of P. sajor-caju coupled
with veratryl alcohol as a redox mediator. Further, three azo
group dyes (reactive black 5, reactive orange 16 and dis-
perse blue 79), two anthraquinone group dyes (disperse red
60 and disperse blue 56) and an artificial textile wastewater
made from all the five reactive and disperse dyes were also
found to be successfully decolourised by crude enzymes
from SMS of P. sajor-caju (Singh et al. 2010). The mech-
anisms of enzymatic decolourisation of dyes were presum-
ably due to laccase and MnP activities, as a recent study
showed that under the induction of malachite green, a triphe-
nylmethane dye, the laccase and MnP levels in the enzyme
extracts of P. ostreatus were increased by 1.4- and 2.1-fold,
respectively, when compared to the controls (Papinutti and
Forchiassin 2010). Summarising, dyes can be removed, de-
graded and detoxified by enzymatic biological process and
also physical adsorption using SMS (Gao et al. 2011; Zhou
et al. 2011). SMS in bioremediation of dye is definitely more
time saving and cost effective.
Acid mine drainage
One of the most widely used organic tools for the bioreme-
diation of acid mine drainage (AMD) is the spent substrates
of mushrooms as it typically contains lime. Passive treat-
ment represents a popular system in remediating AMD.
Briefly, the contaminants are allowed to flow through a
Appl Microbiol Biotechnol (2012) 96:863–873
chemo-bioreactive mixture whereby the organic substrates
(SMS in this case) were bio-augmented with sulphate-
reducing bacteria. With evidences of Cheong et al. (2010)
and Newcombe and Brennan (2010), an uncomplicated
treatment system by using SMS can be a simple and cost-
effective technology to treat AMD effectively.
Mode of action of SMS enzymes
The three common SMS enzymes are lignin peroxidase (LiP,
E.C. 1.11.1.14), Mn-dependant peroxidase (MnP, E.C.
1.11.1.13) and a copper-containing oxidoreductase, laccase
(Lac, E.C. 1.10.3.2). The specificity in terms of substrate
range of the three mentioned lignocellulosic enzymes are
extremely low making them capable of transformation and
metabolism of recalcitrant organo-pollutants analogous to
lignin, for example, PAHs (Pointing 2001). Lignin peroxi-
dases are glycosylated heme proteins and are obligately de-
pendent on H2O2. In the presence of endogenously generated
H2O2, LiP catalyses oxidation of a redox mediator (veratryl
alcohol) in order to generate aryl cation radicals. The free
radicals then carried out diverse reactions, including benzylic
alcohol oxidation, carbon–carbon bond cleavage, hydroxyl-
ation, phenol dimerisation/polymerisation and demethylation
(Reddy and D'Souza 1994; Pointing 2001). On the other hand,
MnPs require Mn (II) for reactivity and catalyse the oxidation
of Mn (II) to Mn (III), which, as a result, oxidises phenols to
phenoxy radicals (Wariishi et al. 1992). LiP-mediated PAH
metabolism is via one-electron oxidation to yield quinone
products, whereas lipid peroxidation-coupled MnP-mediated
PAH oxidation was observed with or without quinone accu-
mulation (Bogan and Lamar 1996; Guenther et al. 1998).
Laccase catalyses oxidation of a broad range of substrates
(e.g., PAHs or recalcitrant dyes) to free radical intermediates
by using molecular oxygen as a final electron acceptor
(Shipovskov et al. 2008). One major limitation of using lac-
case is its low redox potential. However, inclusion of a redox
mediator like ABTS [2,2′-azinobis-(3-ethyl- benzothiazoline-
6-sulfonate)] has overcome the problem and has enabled
a system called “laccase-mediator system”, where the
enzyme-activated mediator (synthetic or natural-occurring
one) undergoes a wide range of reactions with other chem-
icals, making it applicable in bioremediation (Camarero et al.
2005; Cañas et al. 2007). Most recently, Cañas and Camarero
(2010) analysed the different reaction routes during benzo[α]
pyrene oxidations by laccase–ABTS, laccase–HBT (1-
hydroxybenzotriazole) and laccase-PCA (p-coumaric acid).
As a result, it was concluded that laccase–ABTS followed
an electron transfer route, where there was a nucleophilic
attack of the acetate ions towards the benzo[α]pyrene cation
radicals, whereas both laccase–PCA and laccase–HBT fol-
lowed H atom transfer routes.
869
Animal feed
Mushroom substrate used as a growth media to produce
mushroom contains cellulose, lignin and little protein and
thus declared unsuitable for animal feed (Zhu et al. 2012). It
is only after harvesting mushroom that the substrate (now
affirmed “spent”) could be more easily digested by rumi-
nants owing to the enzymatic conversion processes during
mushroom cultivation (Adamović et al. 1998; Streeter et al.
1982). The white-rot fungi degrade lignin and improve the
in vivo dry matter digestibility (IVDMD) of lignocellulosic
materials. Accordingly, crude protein, fat content and ash
content of the spent substrates increase with time but not the
cell wall components (Streeter et al. 1981; Streeter et al. 1982;
Zadrazil and Puniya 1995). With reference to Adamović et al.
(1998), the most notable change of composition in the spent
straw substrate is the reduction of hemicelluloses by 17 %,
cellulose by 15 %, lignin by 4 % and gossypol by 60 % (Zhu et
al. 2012). This leads to the conclusion that all the cell wall
components are being greatly degraded by enzymes secreted
during mycelium growth and mushroom production. This will
directly increase the IVDMD of SMS as a ruminant food. This
finding is consistent with other reports which used Holstein
steers (Ayala et al. 2011) and sheep (Fazaeli and Masoodi
2006) as animal models. Furthermore, SMS also generates a
wealth of polysaccharides, vitamins and some trace elements
such as Fe, Ca, Zn and Mg, which are granted as valuable for
animals (Medina et al. 2009; Paredes et al. 2009; Zhu et al.
2012).
According to Zhang et al. (1995), under solid-state fer-
mentation, the crude protein contents in SMS were also
increased and the in vitro digestibility of the crude protein
was as high as 70 %, thus making SMS a potential source of
nitrogen for poultry and animals. However, not all the
animals tested accepted voluntarily the inclusion of SMS
into the feeding diet. For instance, daily gain of the feeding
trial animals decreased with the presence of compost level
(10 % and 17 %) in the diet, as compared to the control
which had no spent compost (Adamović et al. 1998). Ac-
cordingly, the voluntary intakes were significantly (p<0.05)
reduced when sheep were fed with diet containing 30 % of
SMS from wheat straw, as compared to 10 % and 20 %
formulations (Fazaeli and Masoodi 2006). The voluntary
intake of feeds containing SMS by buffaloes decreased
due to relatively high content of ash (26.4 %) in the diet
(Kakkar et al. 1990; Kakkar and Dhanda 1998). This indi-
cated that ash content at a higher level could deplete the
minerals available in feeds, thus limiting the voluntary in-
take by ruminants. In addition to that, the presence of
phenolic compounds as a result of lignin degradation
through solid state fermentation (and lignin itself) by mush-
rooms could affect digestibility negatively. Nevertheless,
investigations on the effects of supplementation of SMS
870
especially from Pleurotus sp. on rumen feed are still
ongoing by employing different ruminant models like
Holstein calves (Kim et al. 2011a) and Hanwoo steers
(Oh et al. 2010). Kim et al. (2011b), who have recently
worked on spent A. bisporus substrates, reported that
the increased protein contents and decreased fibre con-
tents in the substrates was the impact of mycellial
activity during the A. bisporus mushroom cultivation.
This indicated that SMS could be used as a potential
roughage source for ruminants. The formulation of the
diet of animal feed which includes SMS is not an easy
task, as one must take into account factors like species
of animal, mushroom strains, nutrition level of the SMS,
cell wall component, digestibility and voluntary intake
(Langar et al. 1982). Table 4 summarises the utilisation
of SMS as an animal feed supplement.
Alternative energy
The authors feel it is relevant to discuss the potential use of
enzymes extracted from SMS for alternative energy, that is,
biofuel production and enzymatic fuel cell. Thermal treat-
ment such as combustion of pellets of SMS for energy
recovery (Finney et al. 2009a; Finney et al. 2009b; Ryu et
al. 2008) is not in the scope of this paper, since there is no
enzyme involved. However, SMS as a biofuel feedstock is an
attractive idea for its low cost.
SMS, which has less lignin due to the digestion process
by extra-cellular lignocellulosic enzymes during mushroom
production, is a merit for biofuel production. The lower
lignin content but high nitrogen and ash content make the
SMS more easily digested by microbial degraders to yield
more reducing sugars. Indeed, the resulting polysaccharides
act as a suitable substrate for hydrolysis, since the produc-
tion of SMS itself has served as a form of pre-treatment
Table 4 Utilisation of SMS in animal feed formulation
Mushroom Spent compost
Pleurotus sp., Agrocybe aegarita, Sugarcane bagasse
Pleurotus eryngii, Pleurotus sp. and
Kuehneromyces mutabilis
Lentinula edodes – –
Pleurotus florida Wheat and paddy straw
Agaricus bisporus Rice straw
Wheat straw
Pleurotus ostreatus Wheat straw
Pleurotus sp. Sawdust
Pleurotus eryngii and Pleurotus osteratus Rice straw
Appl Microbiol Biotechnol (2012) 96:863–873
(Hayes and Hayes 2009). Moreover, the conventional raw
materials for the first-generation bioethanol production such
as sugarcane and corn are food and will affect negatively the
cost increment of these substrates. Therefore, SMS which is
a biomass by-product is much favourable and economical.
A study by Asada et al. (2011) has shown that after subject-
ing SMS of L. edodes (shiitake) to steam explosion,
simultaneous saccharification and fermentation, the biocon-
version to ethanol has achieved a theoretical yield of
87.6 %. Oguri et al. (2011) investigated the feasibility of
using the SMS after cultivation of P. eryngii to produce
ethanol. As a result, a high yield of total sugars was obtained
(more than 59.0 %) and upon fermentation, the ethanol yield
was as high as 67.0 %. Collectively, SMS of commercialised
edible mushrooms is an effective renewable biomass re-
source for bioethanol production. Besides that, biogas, a
form of renewable energy resulting from biomass, is now
gaining interest. Biogas generation by SMS of P. sajor-caju
(Bisaria et al. 1990) and Pleurotus florida was high and it
seems to be due to the optimum C/N ratio, thus improving
the susceptibility to digestion of anaerobic fermenters.
Moreover, biocatalyst (enzyme) is now seen as a renewable,
cleaner alternative to conventional metal catalysts for fuel
cell cathodes. Laccase, in particular, has been studied ex-
tensively and most of them are from the white-rot fungus T.
versicolor (Farneth and D'Amore 2005; Farneth et al. 2005).
Laccase extracted from SMS could be used in this enzymat-
ic fuel cell, although in order to realise that, a practical
cathode design and apparatus is needed.
Conclusion
SMS is no longer regarded as a waste but as a renewable
resource from the mushroom industry. Not only can SMS be
employed in a number of green technology endeavours, the
Feeding trial Reference
– Zadrazil and Puniya (1995)
Zhang et al. (1995)
Buffaloes Kakkar and Dhanda (1998)
Kakkar et al. (1990)
Holstein beef cattle Kim et al. (2011b)
Mature castrated male sheep Fazaeli and Masoodi (2006)
Holstein steers Ayala et al. (2011)
Simmenthal heifers Adamović et al. (1998)
Post-weaning calves Kim et al. (2011a)
Hanwoo steers Oh et al. (2010)
Appl Microbiol Biotechnol (2012) 96:863–873
enzymes recovered are potentially useful for the bioremedi-
ation of pollutants and other industrial biotechnology pur-
poses. Having said that, the consistency in performance of
the SMS has to be evaluated and assured in order to realise
the application of SMS and SMS-related products in the
near future.
Acknowledgments This work was funded by the University of
Malaya and the Ministry of Science, Technology and Innovation
(MOSTI) (grant number 01-02-03-1002; 01-02-03-0143). This review
was carried out with the support of a Postgraduate Research Grant
(PV007/2012A).
References
Adamović M, Grubić G, Milenković I, Jovanović R, Protić R, Sretenović
L, Stoićević L (1998) The biodegradation of wheat straw by Pleuro-
tus ostreatus mushrooms and its use in cattle feeding. Anim Feed Sci
Technol 71:357–362
Ahlawat OP, Gupta P, Kumar S, Sharma DK, Ahlawat K (2010)
Bioremediation of fungicides by spent mushroom substrate and
its associated microflora. Indian J Microbiol 50:390–395
Annuar MSM, Adnan S, Vikineswary S, Chisti Y (2009) Kinetics and
energetics of azo dye decolorization by Pycnoporus sanguineus.
Water Air Soil Pollut 202:179–188
Annuar MSM, Murthy SS, Sabanatham V (2010) Laccase production
from oil palm industry solid waste: statistical optimization of
selected process parameters. Eng Life Sci 10:40–48
Asada C, Asakawa A, Sasaki C, Nakamura Y (2011) Characterization
of the steam-exploded spent shiitake mushroom medium and its
efficient conversion to ethanol. Bioresour Technol 102:10052–
10056
Ayala M, González-Muñoz SS, Pinos-Rodríguez JM, Vázquez C,
Meneses M, Loera O, Mendoza GD (2011) Fibrolytic potential
of spent compost of the mushroom Agaricus bisporus to degrade
forages for ruminants. Afr J Microbiol Res 5:241–249
Ayotamuno JM, Okparanma RN, Davis DD, Allagoa M (2010) PAH
removal from Nigerian oil-based drill-cuttings with spent oyster
mushroom (Pleurotus ostreatus) substrate. J Food Agric Environ
8:914–919
Ball A, Jackson A (1995) The recovery of lignocellulose-degrading
enzymes from spent mushroom compost. Bioresour Technol
54:311–314
Barry J, Doyle O, Grant J, Grogan H (2012) Supplementary of spent
mushroom substrate (SMS) to improve the structure and produc-
tivity as a casing material. In: 18th Congress of the International
Society for Mushroom Science. Beijing, China, pp. 735–742.
Benavides J, Rito-Palomares M (2008) Practical experiences from the
development of aqueous two-phase processes for the recovery of
high value biological products. J Chem Technol Biotechnol
83:133–142
Bisaria R, Vasudevan P, Bisaria VS (1990) Utilization of spent agro-
residues from mushroom cultivation for biogas production. Appl
Microbiol Biotechnol 33:607–609
Bogan BW, Lamar RT (1996) Polycyclic aromatic hydrocarbon-
degrading capabilities of Phanerochaete laevis HHB-1625 and
its extracellular ligninolytic enzymes. Appl Environ Microbiol
62:1597–1603
Camarero S, Ibarra D, Martínez MJ, Martínez AT (2005) Lignin-
derived compounds as efficient laccase mediators for decoloriza-
tion of different types of recalcitrant dyes. Appl Environ Micro-
biol 71:1775–1784
871
Cañas A, Alcalde M, Plou FJ, Martínez MJ, Martínez AT, Camarero S
(2007) Transformation of polycyclic aromatic hydrocarbons by
laccase is strongly enhanced by phenolic compounds present in
soil. Environ Sci Technol 41:2964–2971
Cañas AI, Camarero S (2010) Laccases and their natural mediators:
biotechnological tools for sustainable eco-friendly processes. Bio-
technol Adv 28:694–705
Chang ST (1996) Mushroom research and development—equality and
mutual benefit. In: Royse DJ (ed) Mushroom biology and mush-
room products. Pennsylvania State University, University Park,
pp 1–10
Chang ST, Miles PG (1989) Edible mushrooms and their cultivation.
CRC Press, Boca Raton
Chen GQ, Zeng GM, Tu X, Huang GH, Chen YN (2005) A novel
biosorbent: characterization of the spent mushroom compost and
its application for removal of heavy metals. J Environ Sci 17:756–
760
Chen S, Ge W, Buswell JA (2004) Biochemical and molecular char-
acterization of a laccase from the edible straw mushroom, Volvar-
iella volvacea. Eur J Biochem 271:318–328
Cheong YW, Das BK, Roy A, Bhattacharya J (2010) Performance of a
SAPS-based chemo-bioreactor treating acid mine drainage using
low-DOC spent mushroom compost, and limestone as substrate.
Mine Water Environ 29:217–224
Chiu SW, Ching ML, Fong KL, Moore D (1998) Spent oyster mush-
room substrate performs better than many mushroom mycelia in
removing the biocide pentachlorophenol. Mycol Res 102:1553–
1562
Chiu SW, Gao T, Chan CSS, Ho CKM (2009) Removal of spilled
petroleum in industrial soils by spent compost of mushroom
Pleurotus pulmonarius. Chemosphere 75:837–842
Córdova Juarez RA, Gordillo Dorry LL, Bello-Mendoza R, Sánchez
JE (2011) Use of spent substrate after Pleurotus pulmonarius
cultivation for the treatment of chlorothalonil containing waste-
water. J Environ Manage 92:948–952
Eggen T (1999) Application of fungal substrate from commercial mush-
room production—Pleuorotus ostreatus—for bioremediation of cre-
osote contaminated soil. Int Biodeter Biodegrad 44:117–126
Eggen T, Sasek V (2002) Use of edible and medicinal oyster mush-
room [Pleurotus ostreatus (Jacq.:Fr.) Kumm.] spent compost in
remediation of chemically polluted soils. Int J Med Mushrooms
4:255–261
Farneth WE, D'Amore MB (2005) Encapsulated laccase electrodes for
fuel cell cathodes. J Electroanal Chem 581:197–205
Farneth WE, Diner BA, Gierke TD, D'Amore MB (2005) Current
densities from electrocatalytic oxygen reduction in laccase/ABTS
solutions. J Electroanal Chem 581:190–196
Fazaeli H, Masoodi ART (2006) Spent wheat straw compost of Agaricus
bisporus mushroom as ruminant feed. Asian-Aust J Anim Sci 19:
845–851
Finney KN, Ryu C, Sharifi VN, Swithenbank J (2009a) The reuse of
spent mushroom compost and coal tailings for energy recovery:
comparison of thermal treatment technologies. Bioresour Technol
100:310–315
Finney KN, Sharifi VN, Swithenbank J (2009b) Combustion of spent
mushroom compost and coal tailing pellets in a fluidised-bed.
Renew Energy 34:860–868
Gadd GM (2001) Fungi in bioremediation. Cambridge University
Press, Cambridge
Gao JF, Wang JH, Wu XL, Zhang QA, Peng YZ (2011) Protonated
spent mushroom substrate as a potential low-cost biosorbent for
the removal of Reactive Red 15 from aqueous solutions. Fresen
Environ Bull 20:51–62
Gonzalez Matute R, Figlas D, Mockel G, Curvetto N (2012) Degrada-
tion of metsulfuron methyl by Agaricus blazei Murrill spent com-
post enzymes. Biorem J 16:31–37
872
Guenther T, Sack U, Hofrichter M, Laetz M (1998) Oxidation of PAH
and PAH-derivatives by fungal and plant oxidoreductases. J Basic
Microbiol 38:113–122
Hayes DJ, Hayes MH (2009) The role that lignocellulosic feedstocks
and various biorefining technologies can play in meeting Ireland's
biofuel targets. Biofuels Bioprod Bioref 3:500–520
Herrero-Hernández E, Andrades MS, Rodríguez-Cruz MS, Sánchez-
Martín MJ (2011) Effect of spent mushroom substrate applied to
vineyard soil on the behaviour of copper-based fungicide residues. J
Environ Manage 92:1849–1857
Hublik G, Schinner F (2000) Characterization and immobilization of
the laccase from Pleurotus ostreatus and its use for the continuous
elimination of phenolic pollutants. Enzyme Microb Technol
27:330–336
Jordan SN, Mullen GJ, Murphy MC (2008) Composition variability of
spent mushroom compost in Ireland. Bioresour Technol 99:411–
418
Kadian N, Gupta A, Satya S, Mehta RK, Malik A (2008) Biodegrada-
tion of herbicide (atrazine) in contaminated soil using various
bioprocessed materials. Bioresour Technol 99:4642–4647
Kakkar VK, Dhanda S (1998) Comparative evaluation of wheat and
paddy straws for mushroom production and feeding residual
straws to ruminants. Bioresour Technol 66:175–177
Kakkar VK, Garach HS, Dhanda S, Makkar GS (1990) Mushroom
harvested spent straw as feed for buffaloes. Indian J Anim Nutr
7:267–272
Karanasios E, Tsiropoulos N, Karpouzas DG, Ehaliotis C (2010)
Degradation and adsorption of pesticides in compost-based bio-
mixtures as potential substrates for biobeds in South Europe. J
Agric Food Chem 58:9147–9156
Khammuang S, Sarnthima R (2007) Laccase from spent mushroom
compost of Lentinus polychrous Lev. and its potential for remazol
brilliant blue R decolourisation. Biotechnology 6:408–413
Kim M, Lee H, Park J, Kang S, Choi Y (2011a) Recycling of fer-
mented sawdust-based oyster mushroom spent substrate as a feed
supplement for postweaning calves. Asian Australas J Anim Sci
24:493–499
Kim YI, Cho WM, Hong SK, Oh YK, Kwak WS (2011b) Yield,
nutrient characteristics, ruminal solubility and degradability of
spent mushroom (Agaricus bisporus) substrates for ruminants.
Asian Australas J Anim Sci 24:1560–1568
Ko HG, Park SH, Kim SH, Park HG, Park WM (2005) Detection and
recovery of hydrolytic enzymes from spent compost of four mush-
room species. Folia Microbiol 50:103–106
Kumaran S, Sastry CA, Vikineswary S (1997) Laccase, cellulase and
xylanase activities during growth of Pleurotus sajor-caju on sago
hampas. World J Microbiol Biotechnol 13:43–49
Langar PN, Sehgal JP, Rana VK, Singh MM, Garcha HS (1982)
Utilization of Agaricus bisporus-harvested spent wheat straw in
the ruminant diets. Indian J Anim Sci 52:634–637
Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost
to bioremediate PAH-contaminated samples. Chemosphere
52:1539–1546
Law WM, Lau WN, Lo KL, Wai LM, Chiu SW (2003) Removal of
biocide pentachlorophenol in water system by the spent mushroom
compost of Pleurotus pulmonarius. Chemosphere 52:1531–1537
Li X, Lin X, Zhang J, Wang Y (2010) Degradation of polycyclic aromatic
hydrocarbons by crude extracts from spent mushroom substrate and
its possible mechanisms. Current Microbiol 60:336–342
Li Y (2012) Present development situation and tendency of edible
mushroom industry in China. In: 18th Congress of the Interna-
tional Society for Mushroom Science. Beijing, China, pp. 3–9.
Low JYS, Abdullah N, Vikineswary S (2009) Evaluation of support
materials for immobilization of Pycnoporus sanguineus mycelia
for laccase production and biodegradation of polycyclic aromatic
hydrocarbons. Res J Environ Sci 3:357–366
Appl Microbiol Biotechnol (2012) 96:863–873
Low YS, Abdullah N, Vikineswary S (2008) Biodegradation of poly-
cyclic aromatic hydrocarbons by immobilized Pycnoporus san-
guineus on ecomat. J Appl Sci 8:4330–4337
Magette W, Smyth S, Dodd V (1998) Logistical considerations for
spent mushroom compost utilization. In: 8th International Con-
ference on Management Strategies for Organic Waste in Agricul-
ture. Rennes, France, pp. 23–30
Mayolo-Deloisa K, Trejo-Hernández MDR, Rito-Palomares M (2009)
Recovery of laccase from the residual compost of Agaricus bisporus
in aqueous two-phase systems. Process Biochem 44:435–439
Medina E, Paredes C, Perez-Murcia M, Bustamante M, Moral R (2009)
Spent mushroom substrates as component of growing media for
germination and growth of horticultural. Bioresour Technol
100:4227–4232
Mehta V, Gupta JK, Kaushal SC (1990) Cultivation of Pleurotus
florida mushroom on rice straw and biogas production from the
spent straw. World J Microbiol Biotechnol 6:366–370
Molina-Barahona L, Rodríguez-Vázquez R, Hernández-Velasco M,
Vega-Jarquin C, Zapata-Perez O, Mendoza-Cantú A, Albores A
(2004) Diesel removal from contaminated soils by biostimulation
and supplementation with crop residues. Appl Soil Ecol 27:165–175
Mukherjee R, Nandi B (2004) Improvement of in vitro digestibility
through biological treatment of water hyacinth biomass by two
Pleurotus species. Int Biodeter Biodegrad 53:7–12
Munusamy U, Sabaratnam V, Muniandy S, Abdullah N, Pandey A,
Jones EBG (2008) Biodegradation of polycyclic aromatic hydro-
carbons by laccase of Pycnoporus sanguineus and toxicity evalua-
tion of treated PAH. Biotechnol 7:669–677
Nagai M, Sato T, Watanabe H, Saito K, Kawata M, Enei H (2002)
Purification and characterization of an extracellular laccase from
the edible mushroom Lentinula edodes, and decolorization of chem-
ically different dyes. Appl Microbiol Biotechnol 60:327–335
Newcombe CE, Brennan RA (2010) Improved passive treatment of
acid mine drainage in mushroom compost amended with crab-shell
chitin. J Environ Eng 136:616–626
Oei P, Albert G (2012) Recycling casing soil. In: 18th Congress of the
International Society for Mushroom Science. Beijing, China, pp.
757–765.
Oguri E, Takimura O, Matsushika A, Inoue H, Sawayama S (2011)
Bioethanol production by Pichia stipitis from enzymatic hydro-
lysates of corncob-based spent mushroom substrate. Food Sci
Technol Res 17:267–272
Oh Y, Lee W, Choi C, Kim K, Hong S, Lee S, Seol YJ, Kwak WS,
Choi NJ (2010) Effects of spent mushroom substrates supplemen-
tation on rumen fermentation and blood metabolites in Hanwoo
steers. Asian Australas J Anim Sci 23:1608–1613
Pandey A, Soccol CR, Mitchell D (2000) New developments in solid
state fermentation. I. Bioprocesses and products. Process Biochem
35:1153–1169
Papinutti L, Forchiassin F (2010) Adsorption and decolorization of
dyes using solid residues from Pleurotus ostreatus mushroom
production. Biotechnol Bioprocess Eng 15:1102–1109
Paredes C, Medina E, Moral R, Pérez-Murcia MD, Moreno-Caselles J,
Bustamante MA, Cecilia JA (2009) Characterization of the dif-
ferent organic matter fractions of spent mushroom substrate.
Commun Soil Sci Plant Anal 40:150–161
Pointing SB (2001) Feasibility of bioremediation by white-rot fungi.
Appl Microbiol Biotechnol 57:20–33
Poppe J (2000) Use of agricultural waste materials in the cultivation of
mushrooms. Mushroom Sci 15:3–22
Quaratino D, Federici F, Petruccioli M, Fenice M, D'Annibale A
(2007) Production, purification and partial characterisation of a
novel laccase from the white-rot fungus Panus tigrinus CBS
577.79. Antonie Van Leeuwenhoek 91:57–69
Ragunathan R, Swaminathan K (2003) Nutritional status of Pleurotus
spp. grown on various agro-wastes. Food Chem 80:371–375
Appl Microbiol Biotechnol (2012) 96:863–873
Reddy CA, D'Souza TM (1994) Physiology and molecular biology of
the lignin peroxidases of Phanerochaete chrysosporium. FEMS
Microbiol Rev 13:137–152
Rivera-Espinoza Y, Dendooven L (2004) Dynamics of carbon, nitro-
gen and hydrocarbons in diesel-contaminated soil amended with
biosolids and maize. Chemosphere 54:379–386
Royse DJ, Rhodes TW, Ohga S, Sanchez JE (2004) Yield, mush-
room size and time to production of Pleurotus cornucopiae
(oyster mushroom) grown on switch grass substrate spawned
and supplemented at various rates. Bioresour Technol 91:85–
91
Russell M, Basheer PAM, Rao JR (2005) Potential use of spent
mushroom compost ash as an activator for pulverised fuel ash.
Constr Build Mater 19:698–702
Russo L, Rizzo L, Belgiorno V (2012) Ozone oxidation and aerobic
biodegradation with spent mushroom compost for detoxification
and benzo(a)pyrene removal from contaminated soil. Chemosphere
87:595–601
Ryu C, Khor A, Sharifi VN, Swithenbank J (2008) Pelletised fuel
production from coal tailings and spent mushroom compost—part
II. Economic feasibility based on cost analysis. Fuel Process Tech-
nol 89:276–283
Saidu M, Salim MR, Ali M, Yuzir M (2011) Cultivation of oyster
mushroom (Pleurotus spp.) on palm oil mesocarp fibre. Afr J Bio-
technol 10:15973–15976
Shipovskov S, Nimal Gunaratne HQ, Seddon KR, Stephens G (2008)
Catalytic activity of laccases in aqueous solutions of ionic liquids.
Green Chem 10:806–810
Singh AD, Sabaratnam V, Abdullah N, Annuar MSM, Ramachandran
KB (2010) Decolourisation of chemically different dyes by
enzymes from spent compost of Pleurotus sajor-caju and their
kinetics. Afr J Biotechnol 9:41–54
Singh AD, Vikineswary S, Abdullah N, Sekaran M (2011) Enzymes
from spent mushroom substrate of Pleurotus sajor-caju for the
decolourisation and detoxification of textile dyes. World J Micro-
biol Biotechnol 27:535–545
Singh AD, Vikineswary S, Noorlidah A (2002) Extraction of enzymes
from spent compost of Pleurotus sajor-caju and its potential use
for decolourisation of synthetic dye. Mal J Sci 21:9–16
Singh AD, Abdullah N, Vikineswary S (2003) Optimization of extrac-
tion of bulk enzymes from spent mushroom compost. J Chem
Technol Biotechnol 78:743–752
873
Streeter CL, Conway KE, Horn GW (1981) Effect of Pleurotus ostrea-
tus and Erwinia carotovora on wheat straw digestibility. Myco-
logia 73:1040–1048
Streeter CL, Conway KE, Horn GW, Mader TL (1982) Nutritional
evaluation of wheat straw incubated with the edible mushroom,
Pleurotus ostreatus. J Anim Sci 54:183–188
Suguimoto H, Barbosa AM, Dekker RFH, Castro-Gomez RJH (2001)
Veratryl alcohol stimulates fruiting body formation in the oyster
mushroom, Pleurotus ostreatus. FEMS Microbiol Lett 194:235–238
Trejo-Hernandez MR, Lopez-Munguia A, Quintero Ramirez R (2001)
Residual compost of Agaricus bisporus as a source of crude laccase
for enzymic oxidation of phenolic compounds. Process Biochem
36:635–639
Ullrich R, Huong LM, Dung NL, Hofrichter M (2005) Laccase from
the medicinal mushroom Agaricus blazei: production, purification
and characterization. Appl Microbiol Biotechnol 67:357–363
United States Department of Agriculture (2012) Mushroom indus-
try report (94003). http://usda.mannlib.cornell.edu/MannUsda/
viewDocumentInfo.do?documentID01395. Accessed 9 September
2012
Vikineswary S, Abdullah N, Renuvathani M, Sekaran M, Pandey A,
Jones EBG (2006) Productivity of laccase in solid substrate fer-
mentation of selected agro-residues by Pycnoporus sanguineus.
Bioresour Technol 97:171–177
Wariishi H, Valli K, Gold MH (1992) Maganese(II) oxidation by
manganese peroxidase from the basidiomycete Phanerochaete
chrysosporium. J Biol Chem 267:23688–23695
Williams BC, McMullan JT, McCahey S (2001) An initial assessment of
spent mushroom compost as a potential energy feedstock. Bioresour
Technol 79:227–230
Zadrazil F, Puniya AKP (1995) Studies on the effect of particle size on
solid-state fermentation of sugarcane bagasse into animal feed
using white-rot fungi. Bioresour Technol 54:85–87
Zhang CK, Gong F, Li DS (1995) A note on the utilisation of spent
mushroom composts in animal feeds. Bioresour Technol 52:89–91
Zhou Q, Gong WQ, Li YB, Chen SH, Yang DJ, Bai CP, Liu XF, Xu N
(2011) Biosorption of methylene blue onto spent corncob sub-
strate: kinetics, equilibrium and thermodynamic studies. Water Sci
Technol 63:2775–2780
Zhu H, Sheng K, Yan E, Qiao J, Lv F (2012) Extraction, purification
and antibacterial activities of a polysaccharide from spent mush-
room substrate. Int J Biol Macromol 50:840–843