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 Open Agriculture.

2017; 2: 537–543

Review Article

Mustafa Nadhim Owaid*, Anson Barish, Mohammad Ali Shariati

Cultivation of Agaricus bisporus (button mushroom)


and its usages in the biosynthesis of nanoparticles
https://doi.org/10.1515/opag-2017-0056
as possible. It was used as a food and drug (Safwat and Al
received June 10, 2016; accepted August 27, 2017
Kholi 2006) by the Romans who also used various species
Abstract: White button mushroom (Agaricus bisporus), of mushroom in decorating their buildings and places of
Higher Basidiomycota, is a very important nutritional worship (Al-Bahadli and Al-Zahron 1991). The greatest
and medicinal species which is used for recycling agro- developments in mushroom cultivation came from France
wastes including wheat straw, reed plant wastes, waste when Agaricus bisporus was cultivated for the first time in
paper, oat straw, waste tea leaves, some water plants and 1600 A.C. on agricultural media specially prepared for the
others. A. bisporus has many usages in human dietary and purpose (Chang and Miles 2004). Commercial mushroom
pharmaceutical fields due to its composition of essential production was first achieved by a Frenchman in 1780,
amino acids, fatty acids, carbohydrates, low calories, who cultivated A. bisporus underground in quarries near
crude fibers, trace elements and vitamins. Recently Paris (Beyer 2003). Commercial production in USA and
synthesized nanoparticles from A. bisporus were used to Canada has been in place for over 100 years (Al-Bahadli
treat cancer, viral, bacterial and fungal diseases. The goal and Al-Zahron 1991) and in 1894, the first specialized
of this review is to highlight recent data about recycling commission for the development of mushroom cultivation
wastes for Agaricus production and applications of was founded in Pennsylvania, since referred to as the
A. bisporus as a reducing agent in the biosynthesis of silver mushroom capital of the world (Beyer 2003). A. bisporus
nanoparticles. Organically produced foods are currently mushroom is considered to be the most popular
highly desirable, but it can also be used for ecofriendly commercial mushroom grown in the United States and
biosynthesis of nanoparticles. Canada (Halpern 2006). It has a seasonal growth pattern
in China and represents about 70% of the total Chinese
Keywords: agricultural wastes, compost, green chemistry, production (Chen et  al. 2003). There are currently about
nanotechnology, biotechnology 346 growers of Agaricus sp. and specialty mushrooms in
United States and the volume of sales of the mushroom
crop in that year in United States totalled about 450x106 kg

1 Introduction (USDA 2013). The aim of this review is to define the some
of the best growth substrates A.  bisporus, its nutritional
value and its applications in nanomedicine.
Agaricus bisporus, white button mushroom, has long been
targeted by humans foraging for food (Chang and Miles
2004). The ancient Chinese believed in the benefits of 2 Cultivation of A. bisporus on
mushrooms; they believed that the mushroom strengthens
the human body and preserves health and youth for as long
various composts
Mushrooms are considered to be heterotrophic
(saprophytic) organisms and thus possess no chlorophylls,
*Corresponding author: Mustafa Nadhim Owaid, Deapartment of
Heet Education, General Directorate of Education in Anbar, Ministry of
but decompose organic materials to feed off (Chang
Education, Hit, Anbar 31007, Iraq, E-mail: mustafanowaid@gmail.com and Miles 2004). Agaricus bisporus can be cultivated on
Mustafa Nadhim Owaid, Department of Ecology, College of Applied various lignocellulosic materials. Growing and cultivation
Sciences, University of Anbar, Hit, Anbar 31007, Iraq of this species has succeeded on different composted
Anson Barish, University of Goroka, P.O. Box 1078 Goroka, Eastern organic such as chicken, horse or pigeon manures, straw
Highlands Province, Papua New Guinea
residues from wheat, oat, tifton (Andrade et al. 2003) and
Mohammad Ali Shariati, Research Department, LLC, Science and
Education, Russia reed crops (Alkaisi et al. 2016; Rehman et al. 2016), corn

Open Access. © 2017 Mustafa Nadhim Owaid et  al., published by De Gruyter Open. This work is licensed under the Creative Commons
Attribution-NonCommercial-NoDerivs 4.0 License.
538   M. Nadhim Owaid, et al.

cob (Chang and Miles 2004), molasses, wheat bran (Baysal and others. Wheat straw with waste tea leaves (Gulser
et al. 2007), sugarcane bagasse, tea levaves (Simseket al. et  al. 2003; Peker et  al. 2007) and waste paper (Sassine
2008), brachiaria (Brachiaria sp.) (Andrade et  al. 2013), et  al. 2005; Sassine et  al. 2007) were used in the casing
reed plant (Phragmites australis) straw (Muslat et al. 2011), layer. Tables 1-5 showed various compositions of compost
water hyacinth (Eichhornia crassipes) (Reddy et al. 2013) of Agaricus bisporus inform around the world.

Table 1: Manure Compost in USA (Chang and Miles 2004)


Component Proportion of Dry matter (Kg)

Horse Manure 50
Chicken Manure 6
Beer Residues 2.5
Gypsum 1.25
Total weights 59.75

Table 2: Modified Straw Compost in Taiwan (Chang and Miles 2004)


Component Proportion of Dry matter (Kg)

Paddy Straw 85
Urea 1
Ammonium sulfate 2
Super phosphate calcium 3
Potassium sulfate 0.8
Calcium carbonate 2.5
Total weight 94.3

Table 3: Modified Wheat straw composts in Turkey (Colak et al. 2007; Baysal et al. 2007)
Component Proportion of Dry matter (Kg) Proportion of Dry matter (Kg) Proportion of Dry matter (Kg)

Wheat straw 400 400 400


Wheat bran 113 113 113
Ammonium nitrate 17.1 20 15
Urea 10.1 12 10
Molasses 16 16 16
Gypsum 24 24 24
Total weight 580.2 585 578

Table 4: Tea leaf compost in Turkey (Simsek et al. 2008)


Component Proportion of Dry matter (Kg)

Tea leaves 400


Wheat bran 113
Ammonium nitrate 3.67
Urea 2.17
Molasses 16
Gypsum 24
Total weight 559.8

Table 5: Reed straw composts in Iraq (Owaid 2009; Muslat et al. 2014; Owaid et al. 2017)
Dry matter (Kg) Wheat straw compost Reed straw compost Mixture compost (1:1)

Wheat straw 11.316 - 5.658


Phragmites australis Reed straw - 11.376 5.688
Chicken manure 9.331 9.331 9.331
Urea 0.560 0.560 0.560
Gypsum 1.440 1.440 1.440
Total weight 22.647 22.707 22.677
C:N Ratio 9.5:1 21.7:1 20.3:1
 Cultivation of Agaricus bisporus (button mushroom) and its usages in the biosynthesis of nanoparticles   539

Also, new techniques like the new Garbage Automatic 4 Nutritional value of Agaricus
Decompose-Extinguisher (GADE) were used to produce
composts for cultivating and producing A.  bisporus
bisporus
and Pleurotus ostreatus with the highest growth and
In addition to proteins/amino acids (Muslat et al. 2014),
rate of spinning (Sakae et  al. 2006). A.  bisporus has a
carbohydrates, fats, crude fibers, vitamins (Irazoqui
significant role in producing lignin degradation enzymes
et al. 1997), and macro and micro elements (Owaid 2015).
(manganese peroxidase and laccase) (Bonnen et al. 1994)
An important level of phosphorus is present in Agaricus
and is a ready source of enzymes, including laccase
sp. Generally, the percentage of proteins varies from
which is important in polyphenol oxidation (Hou et  al.
34% to 44% of the total dried matter of fruiting bodies
2004). Recent work showed this enzyme was secreted by
of A. bisporus (Grube et al. 2001). Total free amino acids
partnering A.  bisporus and Trichoderma sp. to increase
are 77.92 g/kg; the content of monosodium glutamate-
the production of this enzyme in agricultural composts
like components 22.67 g/kg (Tseng and Mau 1999).
(Flores et al. 2009). Spent mushroom composts have been
A.  bisporus has a complex mix of unsaturated fatty
found to be useful in organic agriculture (Beyer 2003). In
acids including stearic, oleic, linoleic and palmitic acid
figure 1, the zones of composting temperatures were listed.
(Sadler 2003). The contents of fructose, mannitol, and
The temperature inside the pile rises to 60°C whereas the
other reducing sugars are 26.2, 236.2 and 57 g/kg (dry
degrees from 40 to 50°C are suitable for decomposition
weight), respectively.
(Owaid 2009).
Commercially, A. bisporus is used in in fresh , dried
or canned form (Bernas et  al. 2006). The percentage of
3 Benefits of Mushroom dry weight A.  bisporus fruits grown on the wheat straw
compost is about 8-10% (Colak et  al. 2007). Tsai et  al.
The six major constituents of mushrooms are water, (2007) remarked that content of carbohydrate in its fruits
proteins, carbohydrates, fiber, fat, and ash along with ranged from 38-48%, crude protein was 21-27%, crude
minerals and essential amino acids (Heleno et  al. 2010; fiber 17-23.3, crude ash 8-11.00%, and fat 3-4%based on
Alispahic et al. 2015). Mushrooms are a low-costfoodand dry matter. Goyal et  al. (2015) referred to crude fibers of
important source of protein in the fight against A. bisporus being a good source of dietary fibers because
malnutrition. The antioxidant and antibacterial have they help to prevent many of the common diseases like
the ability to prevent damage which is attributed to free obesity disease due to its low calorie content which up
radicals Rhodes, phenolic compounds, etc. (Aida et  al. to 30 calories per 100 grams (fresh) (Al-Bahadli and
2009; Barros et al. 2007). They are also considered to be Al-Zahron 1991).
able to reduce cholesterol and releve stress and certain A.  bisporus is a good source of vitamins, such as
diseases (Bahl 1983). A, B1 (thiamine), B2 (riboflavin), B3 (niacin acid), B5

Figure 1: Pattern of compost zones used in an outdoor composting process outdoor (Beyer 2003)
540   M. Nadhim Owaid, et al.

(pantothenic acid), C (ascorbic acid), D and folic acid 6 Biosynthesis of silver nanopartic-
(Breene 1990, Irazoqui et  al. 1997). It has essential
amino acids useful as a food for human health including
les using Agaricus bisporus
Cystine, Methionine, Threonine, Valine, Isoleucine,
Biosynthesis of metallic nanoparticles has been
Leucine, Lysine, Tyrosine and Phenylalanine (Muslat
developed using edible and medicinal mushrooms. This
et  al. 2014; Tseng and Mau 1999; Mattila et  al. 2002).
has a distinct advantage over chemical methods such as
A.  bisporus contains K, Fe, Zn, Cu, Na, Se, Co and Mn
their biosafety, non-toxicity and being highly ecofriendly
(Irazoqui et  al. 1997; Owaid 2015). Four elements (K,
(green chemistry). This type of the nanoparticle synthesis
P, Ca and Mg) contribute 97-98% of the total element
by edible and medicinal mushrooms is cheap and suitable
concentration of A.  bisporus (Vetter et  al. 2005).
to apply in nanomedicine because of the huge number of
Selenium level of A. bisporus (2.3–2.7 mg kg–1, dry weight)
fruiting bodies which are produced in the world (Owaid
is a useful Se-supplement. Some studies demonstrate
and Ibraheem 2017).
clearly that the Cd and As levels of this species are low
Further ‘green chemistry’ studies have recorded
enough not to present a toxicological risk (Muszynska
biosynthesis of metallic nanoparticles from A.  bisporus
et al. 2015).
mushroom, especially silver nanoparticles (AgNPs) from its
fruiting bodies or mycelia. The biosynthesized nanoparticles
5 Medicinal value of Agaricus from A. bisporus were used in biomedical applications such

bisporus as antibacterial, antifungal, anti-yeast, and antioxidant


activities as shown in Table 6. A.  bisporus had the next
best level of activity (about 11%) after oyster mushrooms
Medicinal mushrooms like Agaricus bisporus have a
(Pleurotus sp.) in the synthesis of metallic nanoparticles in
long history in many traditional therapies. The use of
the last twelve years (Owaid and Ibraheem 2017).
A. bisporus extracts for its bioactivity such as antioxidants
Sudhakar et al. (2014) reported the most efficient eco-
(Javan et al. 2015), antibacterial activity (Jain et al. 2013),
friendly method for biosynthesis of AgNPs from crude
anticancer and anti-inflammation are increasing with
extracts of A. bisporus had distinctive characteristics, such
advantages recently demonstrated in the fight against
as good catalytic, conductivity and chemical stability with
coronary heart diseases, diabetes mellitus, bacterial and
sizes ranged from 15 to 20 nm and spherical shape. Also,
fungal infections, immune system disorders and cancers
an­tibacterial activity of the synthesized A. bisporus-AgNPs
(Dhamodharan and Mirunalini 2010). Dhamodharan and
was investigated by Mirunalini et al. (2012) against Gram-
Mirunalini (2010) reported the therapeutic properties of
positive bacteria like Staphylococcus aureus by using
this mushroom and its biomedical applications in human
disc diffusion test. Silver nanoparticles from A.  bisporus
health care and treatment of chronic inflammations and
have fungicide effect toward Aspergillus niger (Narasimha
cancers.
et  al. 2013). The synergistic effect of A.  bisporus-AgNPs
The Canadian Cancer Society selected A.  bisporus
with some antibiotics like Gentamycin and Ceftriaxone
mushroom because of its effectiveness against human
created a microbial inhibition zone of 26 mm and 25
diseases. A. bisporus has important actions against breast
mm, respectively (Ul-Haq et  al. 2015). Also, AgNPs of
cancer, prostate cancer, and high blood pressure (MC
A.  bisporus had antibacterial activity against multi-drug
2007). This mushroom has been considered an important
resistant bacterial pathogens such as S. typhi, Proteus
medical source for thousands of years (Schmidt 2006),
sp., Enterobacter sp. and Klebsiella sp. (Dhanasekaran
as referred by Roberts et  al. (2008) who reported that
et  al. 2013). However, chitosan NPs of A.  bisporus had
ultraviolet irradiation of fruiting bodies of A. bisporus in
antioxidant effects. All potential antioxidant properties
dosages recommended by Processed Foods Research Unit
reflect a positive anticancer effect (Dhamodharan and
(PFRU) leads to the accumulation of significant quantities
Mirunalini 2010; Dhamodharan and Mirunalini 2013).
of vitamin D2 essential for bone health. and has potential
Eco-friendly nanoparticles were produced from gold salts
for enhancing human immunity and defense mechanisms
like fungal culture filtrate of Pleurotus sapidus Quel and
against microbial invasion and tumor development (Ren
Agaricus bisporus as the reducing and stabilizing agent
et al. 2008). The mushroom’s Lectincontent may be helpful
with average size 65.5 nm (Eskandari-Nojedehi et al. 2016;
to prevent spread of cancer epithelial cells (Halpern 2006),
Sarkar et al. 2013). Finally, ZnS nanocrystals of A. bisporus
and is increasingly effective against oxidation by Selenium
had potential applications in nano-tuned devices
(MC 2007) and Ergothioneine which is not broken by heat
(Senapati et al. 2015).
or cooking (Dubost et al. 2006).
 Cultivation of Agaricus bisporus (button mushroom) and its usages in the biosynthesis of nanoparticles   541

Table 6: Biosynthesis nanoparticles by using A. bisporus (white button mushroom)


Localization Metal Size (nm) Shape Biomedical applications References
synthesis
Intracellular Ag 80-100 Spherical Antibacterial Activity Dhamodharan and Mirunalini 2012

Extracellular Ag ≤30 Spherical Antibacterial and antifungal Activities Sudhakar et al. 2014

Extracellular Chitosan ND ND Antioxidant Activity Dhamodharan and Mirunalini 2010

Extracellular Ag ≤20 Spherical Antibacterial Activity Praveen et al. 2011

Extracellular Ag ND ND Antibacterial Activity Dhanasekaran et al. 2013

Extracellular Ag ND ND Antibacterial Activity Sujatha et al. 2013

Extracellular Chitosan ND ND Antioxidant Activity Dhamodharan and Mirunalini 2013

Extracellular Ag ≤40 Dispersed Antibacterial Activity Ul-Haq et al. 2015

Extracellular Au <33 ND Antibacterial Activity Eskandari-Nojedehi et al. 2016

Extracellular ZnS 3-200 Cubic Nano-tuned Devices Senapati et al. 2015

Extracellular Au 25 spherical Antifungal Activity Eskandari-Nojedehi et al. 2017

Extracellular Lectins ND ND Drug delivery and cancer therapy Majumder 2017

Legend: ND: Non-detected.

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