Open Agriculture. 2017; 2: 537–543

Review Article

Mustafa Nadhim Owaid*, Anson Barish, Mohammad Ali Shariati Cultivation of bisporus (button ) 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 Abstract: White button mushroom (Agaricus bisporus), of mushroom in decorating their buildings and places of Higher , 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, , low calories, who cultivated A. bisporus underground in quarries near crude fibers, trace elements and . 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 and biosynthesis of nanoparticles. Canada (Halpern 2006). It has a seasonal growth pattern in 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 in United States and the volume of sales of the mushroom crop in that year in United States totalled about 450x106 kg (USDA 2013). The aim of this review is to define the some 1 Introduction 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: [email protected] 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, , 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 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 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 in its fruits proteins, carbohydrates, fiber, , 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 (), B3 ( acid), B5

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

(), 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 as antibacterial, antifungal, anti-yeast, and antioxidant bisporus 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 D essential for bone health. and has potential 2 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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