Mushroom Review Paper 2018

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Environmentally sustainable applications of agro-based spent mushroom


substrate (SMS): an overview

Article  in  Journal of Material Cycles and Waste Management · July 2018


DOI: 10.1007/s10163-018-0739-0

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Journal of Material Cycles and Waste Management (2018) 20:1383–1396
https://doi.org/10.1007/s10163-018-0739-0

REVIEW

Environmentally sustainable applications of agro-based spent


mushroom substrate (SMS): an overview
Fatimah Hafifah Mohd Hanafi1 · Shahabaldin Rezania2   · Shazwin Mat Taib1 · Mohd Fadhil Md Din1,3 ·
Masahito Yamauchi4 · Mariko Sakamoto4 · Hirofumi Hara5 · Junboum Park2 · Shirin Shafiei Ebrahimi6

Received: 27 January 2018 / Accepted: 23 April 2018 / Published online: 27 April 2018
© Springer Japan KK, part of Springer Nature 2018

Abstract
Agricultural wastes such as lignocellulosic residues are renewable resources can be used for mushroom cultivation. Spent
mushroom substrate (SMS) is defined as leftover of biomass generated by commercial mushroom industries after harvest-
ing period of mushroom. Mushroom cultivation using agricultural wastes promises a good quality of SMS for producing
beneficial products such as animal feeding and fertilizers. Based on the published papers, the major applications of SMS are
animal feedstock, fertilizer, energy production and wastewater treatment. For instance, some species of mushroom such as
Pleurotus spp. and Agaricus bisporus are suitable for applications of ruminant feedstock and fertilizers. This paper reviews
the recent studies about the beneficial usage of SMS which is considered as a waste since 2013.

Keywords  Agricultural wastes · Spent mushroom substrate · Applications · Animal feedstock · Fertilizer

Introduction as empty fruit bunch (EFB), trunks, palm kernel shells, and
palm fiber [2]. Many Asian countries generate huge amounts
Agricultural waste is defined as residues that remain after of agricultural waste such as palm oil waste, paddy straw,
agricultural activities prior or after processing. They are sugarcane bagasse, corncob, EFB, cottonseed hulls, wheat
also named as “lignocellulosic” and consists of three types straw, hay, and cocoa hulls [3]. Malaysia, China, India, and
of polymer; cellulose, hemicellulose, and lignin [1]. Some Ireland are the dominant mushroom producer countries. In
examples of agricultural wastes are straw, wheat, corncob, Malaysia, the demand for mushroom is about 50 tons per
and waste products from oil palm plantation activities such day, while the current production is only 24 tons per day.
In 2012, approximately 2.71 million tons of fresh mush-
rooms and 3.11 million tons of dried mushroom have been
* Shahabaldin Rezania imported from China to Malaysia [4].
shahab_rezania89@yahoo.com As reviewed by Phan and Sabaratnam [5], an average
1
Department of Environmental Engineering, Faculty production from each mushroom farm is 100 tons of fresh
of Civil Engineering, Universiti Teknologi Malaysia, mushrooms annually. China is one of the biggest mush-
81310 Johor Bahru, Malaysia room producers by 1.5 million tons per year and expected
2
Department of Civil and Environmental Engineering, Seoul to increase the production up to 65% in next 10 years [6]. In
National University, Seoul, Republic of Korea Ireland, the production of the mushroom has started since
3
Centre for Environmental Sustainability and Water Security 1980s while they found a method to produce high-quality
(iPASA), Research Institute for Sustainable Environment, mushroom at low cost that was competitive in European
Universiti Teknologi Malaysia, 81310 Johor Bahru, Malaysia markets [7]. These countries generate tons of agricultural
4
Kagoshima National College of Technology, 1460‑1 Sinko, waste, which is potentially to be used as mushroom sub-
Hayato‑cho, Kirishima‑shi, Kagoshima 899‑5193, Japan strates for high-quality mushroom production. Table 1 shows
5
Malaysia‑Japan International Institute of Technology, the production rate of agricultural waste in some mushroom
Universiti Teknologi Malaysia Kuala Lumpur, Jalan producer countries.
Semarak, 54100 Kuala Lumpur, Malaysia
Based on Table 1, production rate of agricultural wastes
6
Faculty of Education, Universiti Teknologi Malaysia, in mushroom countries producer is in critical level, which
81310 Johor Bahru, Malaysia

13
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1384 Journal of Material Cycles and Waste Management (2018) 20:1383–1396

Table 1  The production rate of agricultural wastes in some mushroom producer countries


Type of agricultural waste Production rate (tons) Management method Year Country References

Paddy straw and citric bagasse 80 N/A 2006 Uruguay [8]


Sugarcane bagasse 250 N/A 2009 India [9]
Empty fruit bunch (EFB) 76.9 million Disposed in plantation 2012 Indonesia [10]
1.88 2013 Malaysia [11]
Palm kernel shells 0.61
Maize, sorghum, millet, rice, cowpea 918 Burning 2016 Nigeria [12]
Spent mushroom substrate (SMS) 4 million Burning 2007 China [13]
210 Disposal, burning and composting 2010 South Korea [5]
[14]
3 million 2017 Europe

can have negative effect to the environment. This huge increased and around 5 million tons of SMS are generated
amount of agricultural waste is difficult to handle and dis- as solid waste annually [19]. About 660,000 tons of Pleu-
carded by disposal and burning methods. By the way, the rotus eryngii SMS are produced in Korea, annually [21].
application and facilities for recycling waste are still lim- The majority of SMS is either spread on the farm land as
ited, then alternative methods for utilizing these agricultural fertilizer or disposal on land or incineration [7]. In regard to
wastes are needed to avoid environmental pollution associ- this concerns, mushroom industries and researchers are still
ated with current disposal methods [15]. looking for the low-cost potential application of SMS with
the low environment pollution that can have some benefits
for them. Therefore, this paper reviews the major applica-
Spent mushroom substrate (SMS) tion of SMS which are animal feedstock, fertilizer, energy
production and wastewater treatment.
Spent mushroom substrate (SMS) are generated abundantly
in the farm after harvesting period of mushroom fruiting
bodies [16]. SMS refers to the biomass waste generated Mushroom species
from mushroom production. Approximately, 5 kg of SMS
is produced for each kilogram of fresh mushroom [17, 18]. Mushroom cultivation using agricultural wastes as substrates
SMS residue is often discarded as a waste after harvesting is able to minimize the environmental pollution in planta-
mushroom in many countries [19]. The amount of SMS in tions and farms. The used cultivation techniques are differ-
mushroom farm is the biggest challenge for disposal man- ent in each country and each type of mushroom substrate
agement [20]. Figure 1 shows the SMS management process [11, 22]. The utilization of low value agricultural waste for
in the mushroom industry. improving nutritional quality of mushrooms has become a
The concerns of SMS disposal was increased since key research priority in the recent past [23]. Many research-
three decades ago. Also, the trend of mushroom production ers are doing research on mushroom cultivation using

Fig. 1  SMS management pro-


cess in the mushroom indus-
try Adopted from Phan and Mushroom harvesting
Agricultural wastes Mushroom substrate
Sabaratnam [5]
finished

Animal feeding Potential Spent mushroom


Fertilizer applications substrates (SMS)
Energy
Wastewater
treatment

Disposal in situ and


incineration

13
Journal of Material Cycles and Waste Management (2018) 20:1383–1396 1385

agricultural waste for various species of mushroom such as grow on diverse agricultural wastes [25]. A. bisporus and L.
Pleurotus spp., Flammulina velutipes, Volvariella volvacea, edodes are dominant mushroom species cultivated in world-
and Lentinula edodes [24, 25]. wide [5]. It is favor in Asia as a medicinal mushroom, and
It has been proved that many types of mushroom can be also can be find in other regions like North America and
cultured on different types of agricultural waste. Corn waste Europe [35]. Table 2 shows the different types of substrate
are known as good sources for production of mushroom [26]. for mushroom cultivation.
In India, corn cob had been widely used as main mushroom
substrate and proved as better substrate since it is available
to achieve approximately 93.75% of biological efficiency of Composition of SMS
mushroom when compared to other substrates [27].
Paddy straw is commonly used mushroom substrate in SMS composition is a very significant to be use as different
cultivation and production of Pleurotus spp. since a decade applications. As studied by Lee et al. [43] main mushroom
ago [28]. Mushrooms are cultivated in over 60 countries substrate can be used in addition with agricultural wastes
such as China, Japan, The Netherlands, Spain, Malaysia, which has better mushroom yield compared to sawdust
and other countries. China is the world’s largest producer substrate. Sawdust-based SMS consists of high amount of
and exporter of edible mushroom such as Pleurotus spp., NDF, ADF, hemicellulose, cellulose, lignin, carbohydrate,
L. edodes and Agaricus bisporus [5]. The number of edible crude protein (CP), ether extract (EE), ash, dry matter (DM),
mushroom (macro fungi) is estimated around 2000 types calcium (Ca), and phosphorus (P) [44]. Meanwhile, paddy
[29] and the genus Pleurotus comprises 40 different species straw-based SMS have enough nutrients such as higher DM
which known as “oyster mushroom” [30]. For instance in and CP and a little lower NDF [13]. Research by Harith et al.
India, the most cultivated mushrooms species are A. bispo- [45] showed that agro-waste have high carbon and nitrogen
rus, P. sajor caju and Volvariella volvacea, while the highest content resulting in better performance of mushroom fruit-
production is A. bisporus by 90% [31]. ing bodies. For example, application of SMS for fertilizer
There are many types of mushroom such as oyster mush- needs consideration to ensure the nutrients are in acceptable
room (P. flabellatus); grey oyster mushroom (P. sajor caju), range. The nutrient composition of spent mushroom sub-
king oyster mushroom (P. eryngii), white oyster mushroom strate with regarding mushroom species is shown in Table 3.
(P. florida), and other mushroom such as white button mush-
room (A. bisporus), shiitake (L. edodes), straw mushroom
(V. volvacea) and wild mushroom (wild sp.) [4, 32]. The Application of spent mushroom substrate
most popular cultivated mushroom are Pleurotus spp. such (SMS)
as P. sajor caju, P. eryngii and P. florida [33, 34]. These
species are very well-known in Asian countries due to its Animal feedstock
effortless cultivation [5]. Pleurotus spp. mostly cultivated
in tropical regions and does not require any intensive care Several types of lignocellulosic biomass such as paddy
or specific temperature. Recently, Pleurotus spp. has gained straw, wheat straw and barley straw have been used as
popularity due to its high nutritional value and ability to ruminant feedstock that contains high amount of nutrients

Table 2  Different types of substrate for mushroom cultivation


Substrates Mushroom types References

Paddy straw, wheat straw, sugarcane bagasse P. pulmonarius [36]


Paddy straw Volvariella volvacea [37]
Weed plants; palm kernel cake and maize cob; palm kernel cake and sawdust; maize straw and sawdust P. ostreatus [26]
[38]
Sawdust substrates (Mango, Jackfruit, Coconut, Jam, Kadom, Mahogony, Shiris) P. flabellatus [32]
Grass plants such as Panicum repens, Pennisetum purpureum and Zea mays P. citrinopileatus [39]
Rubber trees sawdust and paddy straw P. eryngii [34]
Paddy straw P. sapidus [40]
Paddy straw, wheat straw, sugarcane bagasse; corncob; fruits and vegetables peels (sweet lime, water- P. florida [27]
melon, banana) [36]
Paddy straw, wheat straw, sugarcane bagasse, tea waste P. sajor caju [22]
[41]
Onion wastes P. sajor caju [42]

13

1386 Journal of Material Cycles and Waste Management (2018) 20:1383–1396

[55, 56]. Ruminants are herbivores which can digest large

References
amount of plant that suits for their digestive system [57]. For
example, cattles are more likely to eat paddy straw; however,

[46]
[47]
[48]
[49]
[50]
[51]
[52]
[53]
[54]
it has high silica content that weakens the feed digestibility
[58]. Hence, the utilization of paddy straw is limited since

14.43 mg/100 g

Carbo carbohydrates, CP crude protein, CFT crude fat, CF crude fiber, Fe iron, Zn zinc, Ca calcium, Mg magnesium, K potassium, Na sodium, P phosphorus, N/A not available
low digestibility level for ruminant feeding [59, 60].
Mushroom can be used as a part of the normal human

12.10
diet [61, 62]. The consumption rate of mushrooms have been

0.10
N/A
N/A
N/A
N/A
N/A

N/A
P

increased tremendously either in form of fresh or preserved


6.02 [30]. As stated by Van et al. [63] improving the efficiency of

86.0
N/A
N/A

N/A
N/A
N/A

N/A
0.8
Na

production and reducing cost of supplemental for ruminants


are significant for both the smallholder and commercial
149.6

346.0

0.32
N/A
N/A

N/A
N/A
N/A

1.2
dairy farmers. For example, neutral detergent fiber (NDF),
K

acid detergent fiber (ADF), lignin, ash, cellulose, hemicel-


34.92
N/A
N/A

N/A
N/A
N/A
N/A

N/A
Mg

0.2
lulose and protein are essential components of SMS that can
be used as animal feedstock to ensure easy digestibility by
111.40

ruminant [64]. As reviewed by some researchers, one of the


2.08

5.60
N/A
N/A

N/A
N/A

N/A
1.6
Ca

way for usage of SMS is ruminant feeding [55, 56, 65]. Idea
in using SMS as ruminant feedstock started since decades
63.33

0.40
N/A

N/A
N/A
N/A
N/A

N/A

ago using P. ostreatus and L. edodes [22, 66].


Zn

60

Agro-based SMS has much higher ruminal degradabil-


5.56 g/kg

ity and low amount of neutral detergent fiber (NDF) which


(mg/L)

5.62

1.70
N/A

N/A
N/A
N/A
N/A

is suitable to be developed into additional supplement for


200
Fe

ruminant animals [67]. Fazeli et al. [64] found that SMS


16.7
12.0

33.1
12.7

1.87
N/A

N/A

from various species of mushroom are suitable to be used as


9.3

7.5
CF

ruminant feedstock as they contain essential nutrients similar


CFT

to commercial animal pellets. For example, SMS has poly-


2.6
8.4
0.7
5.2
1.0
2.5
2.9
1.7
1.0

saccharides, vitamins and some trace elements such as iron


37.6
21.6
2.4
22.5
12.8
33.7
22.4
12.5
38.1

(Fe), calcium (Ca), zinc (Zn) and magnesium (Mg) which


CP

are adaptable to animals [68, 69]. The content of amino acids


10.2
10.7

1.10
N/A
Ash

and dietary protein plays a crucial role in the ruminants’


9.4
6.1

6.6
4.3

3.6

diets. Results by Park et al. [70] showed that the addition of


Moisture
Nutrient contents

SMS to the diet of elk enhanced the physiological condition


of elk during growth. P. florida straw-based SMS had higher
85.8
88.1

90.0

90.8

90.4
N/A

N/A

N/A
N/A

degradable value compared to P. sajor-caju-SMS, that make


Table 3  Nutrient composition of SMS in different mushroom species

Carbo

it feasible to be used as ruminant feedstock. P. ostreatus corn


31.3

48.2
81.9
20.6
62.9
66.1
42.3
N/A
(%)

3.3

straw-based SMS improved chemical composition of straws


and growth performance of feedlot lambs, without negative
Almond and walnut shells
Button mushroom’s stipe

effects on carcass characteristics [71]. Table 4 shows utiliza-


tion of agro-based SMS in feeding ruminants.
SMS is not an ideal forage for ruminants since the species
Cotton waste

growth did not improve the nutritional quality of the agricul-


Wheat straw

Paddy straw
Bean straw

Date palm
Substrates

tural by-products. As reviewed by Mahesh and Mohini, [76]


to improve the digestion of straws and increase the digest-
N/A

N/A

ibility for the ruminant animals, biological treatment should


be applied. Besides, it is able to increase crude protein, fat
Auricularia auricular-judae

content, ash content and lower the amount of crude fiber


[77]. As reported by Kwak et al. [78] and Ayala et al. [79]
Agrocybe cylindracea
Polyporus tenuiculus

Volvariella volvacea
Types of mushroom

Agaricus bisporus

SMS from A. bisporus species has a high fibro lytic activ-


Lentinula edodes

ity, which can increase degradation of forages for ruminant.


Pleurotus spp.

Some types of SMS are incompatible to be used as rumi-


nant feedstock due to its low nutrient composition, hence,
might need some modification. Hence, it needs to undergo

13
Table 4  Utilization of agro-based SMS in feeding ruminants
Type of mushroom Substrates type Finding Remarks Feeding trial References

N/A Microbially-fermented SMS Feeding microbially fermented SMS Microbially fermented SMS had 24 to 40 kg Hanwoo steers [21]
improved growth performance and charac- of higher weight in finishing period com-
teristics pared to control group
Agaricus bisporus Wheat straw, poultry manure, calcium sul- Wheat straw based-SMS can be used in the Negatively affect the feed intake and daily Calves [64]
fate, sugar beet molasses and urea diet of finishing calves in pellet form gain when the feed offered as total mixed
ration in mash form
Pleurotus ostreatus Sawdust-based SMS SMS can replace wheat bran in broilers High fiber content of SMS Broilers [72]
production Increased feed intake value of chicks
Journal of Material Cycles and Waste Management (2018) 20:1383–1396

Pleurotus ostreatus Fresh SMS SMS can be used instead of barley in the Decreased final weight of ruminant with Awassi lambs [67]
ration of 15% without any negative effect increase of SMS dietary ratio
on most of carcass characteristics
N/A Sawdust, beet pulp, corncobs, and cottonseed Sawdust-based SMS was successfully ensiled L. plantarum KU5 with combination of N/A [73]
meal with L. plantarum KU5 inoculant and molasses improved the aerobic stability of
molasses for animal use sawdust-based SMS for animal feed
Flammulina velutipes Fresh SMS SMS-based silage supplemented with or Feeding Holstein steers with SMS-based Holstein steers [74]
without urea decreases the protozoa popu- silage significantly decreases protozoa in
lation, and methane emission the rumen
Pleurotus ostreatus Fresh SMS Ruminal disappearance of SMS ensiled with Fresh SMS with L. brevis can replace Hanwoo steers [75]
L. brevis were slightly higher compared to formulated feeding pellets as cost-effective
fresh SMS feeding

N/A: the findings for these journals are focused on the utilization of SMS only

13
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1388 Journal of Material Cycles and Waste Management (2018) 20:1383–1396

some biological treatment to improve the nutrient compo- the potential to be used as a micronutrient fertilizer. In addi-
sition as well as ruminal digestibility. Due to the complex tion, SMS can be converted into micronutrient fertilizer by
relationship of rumen microorganism, conformation, and bio-sorption process that resulted in improvement of soil
biological activity further studies are still needed [80]. SMS structure, quality, and its sorption capacity [97]. Table 5
can be used in combination with conventional roughage for summarizes the mixtures or improved agro-based SMS as
improvement of forage quality, in Asian countries. For this bio-fertilizer for different crops cultivation.
issue, a practical large-scaled research needs to be conducted SMS can be integrated using new formulations and meth-
[81]. odologies with the added advantages of lowering produc-
tion cost and minimizing the environmental impact of its
Fertilizer over-growing accumulation. In addition, a further study is
needed to find new biological material drying methods and
SMS contains sufficient nutrients and generally non-toxic new types of the biomass for the production of micronutri-
materials to the plants growth that made it feasible to be used ent fertilizer components. Using this strategy, an increase
as bio-fertilizer [82]. The main components of SMS to use it in the portfolio of new micronutrient fertilizer products and
as fertilizer are calcium, nitrogen, ash, and protein [83, 84]. reduction in production costs is expected [99].
Many studies showed the feasibility of SMS in horticulture
application either alone or with additional of other materi-
als [83, 85]. The reuse of SMSs as soil improvements has Energy
become the focus of attention as it is rich in nitrogen [86].
SMS is able to modify soil structure to prevent the trans- Agro-industrial biomass (lignocellulosic) is renewable,
port of pesticides and/or facilitate their dispersion [87]. For abundant and provides a unique natural resource for bio-
instance, SMS from (Lentinus edodes) is suitable replace- energy production [101]. Usage of SMS for energy produc-
ment for mulch based on the physicochemical characteris- tion provides a sustainable management solution to divert
tics and biological activity on pesticide degradation [88]. SMS from landfill which produce minimal acid gas emission
Besides, it is rich in organic and essential plant nutrients that ­(NOx, ­SOx, and HCl) [102]. Based on literature, application
make it a useful material for soil improvement and mulching. of SMS in energy production is a promising alternative for
The results of 42-day incubation of mushroom cultivation mushroom producers to minimize SMS production on site;
can significantly enhance the mineral nitrogen contained in hence it can promote sustainable growth of mushroom. The
soil [83]. P is a major nutrient for plants growth, therefore, use of SMS in bioethanol production represents a poten-
the application of SMS in improving soils structure can tial mitigation solution for arises environmental issues by
act as an additive of P for soils with high efficiency of bio- mushroom industry [103, 104]. SMS has less lignin due to
fertilizers for plants [89]. SMS is rich in phosphorus and is degradation process during mushroom production which is
always applied to agriculture land to enhance soil organic an advantage for energy production [5]. For instance, com-
matter and nutrient contents [90]. bustion of SMS with combination of coal tailing in pellet
For instance, SMS also can be a bio-fertilizer for the form was efficient (up to 91.7%) when compared to packed-
cultivation of Pleurotus spp. [84]. Many studies were used bed combustion or the use of unpelletized SMS [102]. SMS
SMS to grow crops such as pineapple, tomatoes and lettuce is highly degradable and co-digestion of SMS with wheat
[91–93]. Recently, Meng et al. [94] found that the addition straw was efficient to enhance the methane production [17].
of pig manure to SMS can increase the nutrition content of Also, hydrogen can be produced from SMS using Clostrid-
N, P, and K which make it suitable to be used as fertiliz- ium thermocellum to degrade lignin [105]. As reported by
ers. The pre-treated SMS with alkaline could enhance the Wu et al. [106], SMS contains high yield of reducing sugar
enzymatic saccharification to produce bio-fertilizers [95]. As and can acts as a potential carbon source. Table 6 shows the
reported by Álvarez-Martín et al. [87] all cultivated plants on usage of SMS in energy production.
soil treated with SMS from A. bisporus and Pleurotus spp. Meanwhile, some important factors should be considered
showed significant differences in the yield. Soil treated SMS for energy production using SMS: (1) the type of biomass
can enhance plant yield in compare to non-treated soil by which has direct influence on yield of energy production, (2)
SMS. For example, Zhang et al. [96] obtained higher yield of mushroom species has effect on availability of lignocellu-
tomatoes and cucumber in soil treated with SMS compared losic part of biomass and subsequently sugar ratio, (3) opti-
to non-treated with SMS. This proved that SMS has positive mum ratio of biomass and SMS to enhance production rate,
effect on the growth of the vegetables. Besides, SMS was (4) co-digestion of SMS with suitable lignocellulosic bio-
used as a replacement of mineral fertilizers. Grain yield for mass to increase the yield of energy production. Although,
maize treated with micronutrients by SMS had 11.5% higher the production yield can be decreased due to generation of
yield than non-treated ones. This finding showed SMS has some by-products.

13
Table 5  The mixtures or improved agro-based SMS as bio-fertilizer for different crops cultivation
Type of mushroom Mixture/improved substrates Crops trials Finding Remarks References

Agaricus bisporus SMS and peat moss Kai-lan (Brassica oleracea var. SMS was feasible to replace the SMS alone cannot be used as [82]
Alboglabra) amount of peat moss for pot growing media
culture of Kai-lan, and increased The formula used is 50% SMS and
the cost effectiveness of growing 50% peat moss
media
Pleurotus ostreatus Sawdust-based SMS Pineapple Treated soil with SMS had two Performed better for vegetative [91]
times higher of fruiting bodies parameter and fruiting
compared to the control soil
Agaricus subrufescens Fresh SMS Seedlings and tomato crops Resulted in more vigorous plants, Production yield was higher or at [92]
leading not only greater yields least equal compared to other
and also greater size of fruits types fertilizers
compared to the commercial
control
Hypsizigus marmoreus SMS, cottonseed hulls and wheat Cultivation of Pleurotus ostreatus 25% SMS showed better quality Economically acceptable [98]
bran traits and chemical content com- Reduce disposal rate of SMS
pared with the control samples
Agaricus bisporus Bio-sorption of SMS Maize SMS has the potentials to be used SMS was noticeably higher than [99]
as a micronutrient fertilizer the untreated group and NPK
Journal of Material Cycles and Waste Management (2018) 20:1383–1396

fertilizer treated
Agaricus bisporus, Pleurotus spp. SMS from Agaricus bisporus crop Lettuce Presence of SMS improved soil Resulted in similar yields with [93]
mixed with SMS from Pleurotus fertility while the nutritional mineral fertilizer
crop contents of lettuce plants were
greater than or similar to control
samples
Pleurotus ostreatus Sawdust-based SMS Fluted pumpkin Results showed that SMS Number of vines, vine length, and [100]
had higher value of N, P, K number of leaves was better with
compared to control soil. SMS the presents of SMS compared
improved fluted pumpkin plants to control soils
performance
Pleurotus ostreatus Fresh SMS N/A The addition of fresh SMS to the High porosity and high fractal [85]
soil changed the soil structure dimension
and the porosity in both topsoil SMS modified the soil structure
and subsoil Present of SMS developed granu-
lar aggregates in the soil
Pleurotus spp. SSF treatment of SMS N/A Carbon sources and rock The formula contains great [84]
phosphate used in mushroom nutritional value to be used for
cultivation suitable for later fertilizers
usage of natural fertilizer and  The P. farinose was used as to
soil amender in agriculture and convert SMS into bio-fertilizers
horticulture fields by SSF

13
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1390 Journal of Material Cycles and Waste Management (2018) 20:1383–1396

Wastewater treatment
References
[14] As reported by several studies, SMS is used as an effective
material for treatment of different pollutants from waste-
water [117–119]. For instance, to nitrogen removal from
It can be used as a peat replace-

wastewater, SMS is promising carbon source due to its


ryegrass growth and significantly ment in horticulture activity

efficient characteristics. Also, by addition of SMS, nitro-


gen removal was enhanced from 46.9 to 87.8% [120]. As
found by Karas et al. [121] fresh mushroom substrate of
P. ostreatus was efficient for the removal of ortho-phe-
nylphenol and imazalil from citrus fruit-packaging plants
Remarks

wastewater.
Recently, Jin et al. [122] used immobilized SMS from
Pleurotus ostreatus for removal of Cd(II) from synthetic
improved grass yield up to 300%

wastewater. They found that the bio-sorption capacity was


SMS was able to support Italian

when compared to untreated

dependent to pH value, initial concentration of Cd(II) and


contact temperature in batch system. In conclusion, the max-
imum adsorption capacity was 100 mg/g in accordance with
the Langmuir isotherm model. In another study, SMS from
Auricularia auricular with modification with cetyltrimethyl
ammonium bromide and immobilized by sodium alginate
control

was used as a novel method for the removal of heavy metals


Finding

from industrial wastewater In addition, SMS of A. bisporus,


successfully acted as bio-sorbent in removing heavy metals
like cadmium (Cd) and mercury (Pb). In addition, SMS of
commercialized edible mushrooms is an effective renew-
able biomass resource for treating wastewater in low-cost
operation [123].
A study by Toptas et al. [124] indicates that SMS was
used in batch adsorption, was effective as a low-cost bio-
Italian grass
Crops trials

sorbent in treating dye effluent. In addition, SMS has poten-


tial to be used as an adsorbent to remove methylene blue
N/A: the findings for these journals are stressed on the utilization of SMS only

form wastewater containing cationic dyes [125]. As inves-


tigated by Zhou, et al. [126] SMS from A. bisporus was
developed a strategy to improve volatile fatty acids bio-
production from waste activated sludge and can reduce the
Mixture/improved substrates

operational cost. Asemoloye et al. [127] stated that oyster


mushroom (P. ostreatus) reduced heavy metal and PAH
contents in soil better than control (M. maximus grass). In
conclusion, there are some challenges for wastewater treat-
Wheat straw

ment using SMS. Recently, Nakajima et al. [128] extracted


active enzymes from spent mushroom compost such as Cel-
lulases, β-glucosidase, dextranase, amylase and laccase.
They found that Pleurotus sp. had the highest decolorizing
capacity among tested fungi.
Here are some challenges for application of SMS for
treatment of different type of wastewater. The characteristics
of SMS should be considered and where the mushroom has
Table 5  (continued)
Type of mushroom
Agaricus bisporus

been originated to enhance the adsorption capacity. Mean-


while, it can be expected that adsorbent made from SMS
could not be effective material in high range of pollution in
water. It is assumed that it could not be used in industrial and
refinery wastewater due to specific characteristic.

13
Journal of Material Cycles and Waste Management (2018) 20:1383–1396 1391

Table 6  Application of SMS in energy production


Mixture/SMS Mushroom type Findings Energy References

SMS Shiitake 23.8 g/L ethanol produced with substrate con- Ethanol [107]
centration of 100 g/L
Sorghum-based SMS Pleurotus ostreatus The ethanol yield was 63.9 g/kg dry matter [104]
SMS and kelp seaweed N/A The biochar from co-pyrolysing of SMS with Bio-char [108]
10% kelp seaweed had more oxygen-contain-
ing groups, and exchangeable cations
SMS with pig manure and rice straw N/A SMS-derived biochar was rich in nutrients such [109]
as P, K, Na, and N
SMS-based biochar N/A SMS-biochar reduced 43% of TN and 66% of [86]
COD
Oil shale semi-coke SMS N/A Bio-oil produced from SMS and shale semi- Bio-oil [110]
coke had high carbon and hydrogen content,
and lower oxygen content
SMS with chemical vapor deposition of ­SiO2 N/A The mixture had high oil fraction yield and [111]
toluene and xylene content
SMS N/A Effective H/C ratios above 1 indicated the qual- Biocrude [112]
ity of produced biocrude
SMS with Clostridium thermocellum N/A Addition of SMS resulted in an accumulation of Hydrogen [113]
28% more or 5.06 g/L reducing sugars
SMS N/A Improved sugar yield and reduced lignin con- Butanol [114]
tent. The maximum amount of butanol was
30.21 g/L
Co-digestion of SMS and dairy manure F. velutipes (SFv) SMS was suitable feedstock for biogas produc- Methane [115]
and P. erygii var. tion and high degradability of SMS had influ-
tuoliensis ence on anaerobic digestion
Spent mushroom compost and wheat straw N/A Maximum production was in C/N ratio of 30 at Biogas [116]
temperature of 55 °C by 44.1001 ml/g

N/A: the findings for these journals are stressed on the application of SMS only

Other applications of SMS Conclusion

According to Medina et al. [68] one of the major problems Wide range of mushroom species such as Pleurotus spp., F.
for the mushroom producing countries is the disposal of velutipes, V. volvacea can be cultivated with different agro-
SMS in environmental friendly way to prevent the environ- residues like paddy, rice straw, and grass plants. The lefto-
mental pollution. Also, there is a problem for mushroom ver of mushroom after harvesting (SMS) is suitable to be
industry since it has produced 20% SMS for each 1 kg- used as fertilizer as it is rich in nutrients. By the way, wide
mushroom beds [62]. Application of SMS is not focused range of organic and inorganic compounds and heavy metals
only on ruminant feedstock, fertilizers, energy production can be adsorbed by SMS in the cost effectiveness way. The
and wastewater treatment, but also can be used as potential nutritional quality of SMS also depends on the mushroom
feed additives for aquaculture farmed fish [129]. In another species used on the substrates. For instance, the growth of
study, SMS was suitable in cultivation of fungi in solid state the Pleurotus djamor on maize stover did not improve the
fermentation to produce the enzymes xylanase, amylase, nutritional quality of SMS, hence it is incompatible to be
cellulose and β-glucosidase [130]. As studied by Liu et al. used as ruminant feedstock.
[131], SMS also can be used as antioxidant for the preven- This review shows that agro-based SMS can be used as
tion of diabetes. Table 7 shows other applications of SMS. substrates in mushroom cultivation as well as for several
applications such as animal feedstock, fertilizer, energy pro-
duction, and wastewater treatment. Besides, SMS also can be
used in soil amendment and enrichment, dye-decolorization,
ammonia emission reduction. For future studies, optimiza-
tion on the ratio of substrates for ruminant feedstock and fer-
tilizer is recommended. Although, some research is needed

13

1392 Journal of Material Cycles and Waste Management (2018) 20:1383–1396

Table 7  Other applications of SMS

Substrates type Mushroom type Potential usage References

Sawdust; wheat straw P. ostreatus Degradation of e 1,1,1-trichloro-2,2-bis (4-chlorophenyl) ethane [132]


in contaminated soil
N/A Agaricus bisporus Added as additive for soil amendment to recover copper [133]
Corncob, cotton seed hulls Pleurotus ostreastus SMS hydrolysates production was useful for the production of [134]
high-value compounds such as nisin and lactic acid
N/A P. eryngii, P. cornucopiae Dye-decolorization [135]
Paddy straw P. pulmonarius Treatment of polycyclic aromatic hydrocarbon (PHA) [136]
Cereal straw Agaricus bisporus and P. ostreatus Production of horticultural seedlings [14]
[68]
N/A N/A Leaching fungicide (tebuconazole and cymoxanil) [137]
Enhance mineral composition of soils
N/A N/A Volatile fatty acid production [138]
Sewage sludge, wheat straw N/A Improved the degradation of organic matter and compost quality [139]
N/A Cordyceps militaris Improve growth and health status of Nile tilapia [140]
N/A N/A Degradation of tetrabromobisphenol-A (TBBPA) in sludge [141]
Corn stalk N/A SMS as a bulking agent resulted in improvement of composting [142]
efficiency by shortening the maturity time

N/A: the findings for these journals are stressed on the utilization of SMS only

to find the best biological treatment for ruminant feedstock 8. Alborés S, Pianzzola MJ, Soubes M, Cerdeiras MP (2006) Bio-
that can improve SMS nutritional quality. degradation of agroindustrial wastes by Pleurotus spp. for its
use as ruminant feed. Electron J Biotechnol 9(3). https​://doi.
org/10.2225/vol9-issue​3-fullt​ext-2
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