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Agriculture

Different ways to exploit mushrooms: A review

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Pages 450-460 | Received 14 Oct 2020, Accepted 16 Apr 2021, Published online: 20 May 2021

Abstract

Mushrooms are a nutritionally, economically, and biotechnologically valuable group of organisms. They are packed with nutritional value in the form of low calories, high protein, and fiber contents. Besides being an important source of food, mushrooms are exploited by man in various ways. Mushrooms can be used in the pharmaceutical industry as antioxidant, anticancer, and immunomodulating agents. They are, at the same time beneficial for human beings and forests as nutrient recyclers in the form of natural decomposers. Mushrooms are also the best source to attain sustainable development goals set by the UNO. Food insecurity, malnutrition and pollution are some of the major issues faced by the modern world in the recent era. Mushrooms in the form of mushroom farming are a promising way to overcome these challenges. Mushroom farming is an efficient way for agro-industrial waste disposal and ensures food security. It is also the cheapest source to make up for the deficiency caused by malnutrition. It supports the local economy by providing more opportunities for livelihood and income by local and national trade. The present review emphasizes the comprehensive account of the different aspects of mushrooms exploitation by which it can save the planet earth and people living on it.

Introduction

Mushroom is a macrofungus which possesses distinguishing sporocarp that may be either hypogeous (underground) or epigeous (aboveground) and big enough to be viewable in unaided sight and to be plucked by hand. It was described that 1,60,000 of the 1.5 million known fungi species produce sporocarp of enough sizes and suited structures to be studied as macro fungi or mushrooms (Hawksworth Citation2012; Murugesan Citation2017). Around 7000 of the 16,000 recognized mushroom species (Hawksworth Citation2012) exhibit different ranges of edibility, about 3000 species are primary edible mushrooms, and around 700 are considered as healthy therapeutic mushrooms (Chang and Wasser Citation2017; Li et al. Citation2021).

There are 200 mushroom species being utilized as superfood throughout the world (Kalac Citation2013); out of which only 35 species are commercially cultivated and 10 have attained the status of industrial production in several countries. (Aida et al. Citation2009; Xu et al. Citation2011; Chang and Wasser Citation2017). In 1978, a Frenchman first achieved commercial production of mushroom who propagated Agaricus bisporus belowground in quarries nearby Paris. The early functional committee for the exploitation of mushroom farming was developed in Pennsylvania in 1894, since considered as the mushroom center of the world (Beyer Citation2003). Different groups of mushrooms such as mycorrhizal, saprophytic, and parasitic are present in nature but saprophytic mushrooms are usually preferred for artificial cultivation (Stamets Citation2000) such as Pleurotus ostreatus (Jacq.) P. Kumm., Agaricus bisporus (J.E. Lange) Imbach, Lentinula edodes (Berk.) Pegler, Hypsizygus marmoreus (Peck) H.E. Bigelow, Auricularia auricula-judae (Bull.) Quél, Flammulina velutipes (Curtis) Singer, Volvariella volvacea (Bull.) Singer, Grifola frondosa (Dicks.) Gray, Pholiota nameko (T. Ito) S. Ito & S. Imai, and Tremella fuciformis Berk (Miles and Chang Citation2004). These mushrooms consist of four influential nutrients including glutathione, selenium, ergothioneine, and vitamin D that are identified to serve as antioxidants and alleviate oxidative tension (CNN Health Citation2018). Mushrooms may exhibit health-promoting qualities with antihyperlipidemic activity (Opletal et al. Citation1997), antigenotoxicity (Wang et al. Citation2005), anti-tumorigenic (Kim et al. Citation2015), hypocholesterolaemic activity (Han et al. Citation2011), antifungal activity (Ye et al. Citation1999), immunostimulation (Vaz et al. Citation2011), anti-nociceptive, anti-hypertensive, immunostimulation (Vaz et al. Citation2011), antioxidation (Roupas et al. Citation2012), stress-relieving characteristics and is also effective for diabetic sufferers (Akata et al. Citation2012). Another valuable attribute of the cultivation of mushrooms is to curtail pollutants in the surroundings. It plays its role in the bio-transformation of lignin and cellulosic residues of foodstuff and the valuable product have rendered a substantial influence on national and regional pollution ranges and will remain to rise (Chang and Miles Citation1984). Mushroom cultivation technology is quite a recent revolution. The economic and social position of poor farmers can be improved by the addition of this non-conventional crop in subsisting agricultural systems. After yeast, mushrooms cultivation is referred to as the largest economical microbial technology (Pathak et al. Citation2009). Due to this technology, the worldwide production of mushrooms and truffles raised from 6.90 to 10.24 million metric tons during the past 10 years (Ho et al. Citation2020). The Global influence of medicinal and edible mushrooms on human well-being is considered as a step towards the non-green revolution (Chang Citation1999).

Significance of uptake of mushrooms has been raised now more than ever during the pandemic SARS-CoV-2 because there is no specific treatment or vaccine is available to fight against it but by the regular intake of natural products like Inonotus obliquus, lentinula edodes, and Grifola frondosa with effective antiviral and anti-inflammatory peculiarities, effects of SARS-CoV-2 can be minimized (Shahzad et al. Citation2020). The main aim of this review is to describe different aspects of medicinal and edible mushroom by which it has revolutionized the world; a step toward the non-green revolution.

Nutritional and therapeutic values

Mushrooms are acknowledged not only because of their flavor and texture but also due to their nutritional and chemical properties (Beluhan and Ranogajec Citation2011).

According to the report of Global Hunger Index (Citation2019), African and Asian countries are challenging a huge hunger and malnutrition problem. The Sustainable Development Goals (SDGs) of the United Nations require governments worldwide to end hunger, attain food security and upgrade nutrition by 2030, particularly for the poor and vulnerable parts of society including infants. Current figures indicate that nearly 690 million people, or 8.9% of the world’s population.is ill fed. Asia has the largest number of undernourished (381 million) followed by Africa (250 million), Latin America and the Caribbean (48 million) (WHO Citation2020).

Cultivated mushrooms are enriched with the proteins, minerals contents, vitamin K, B vitamins, vitamin D, and occasionally vitamins A and C while being low in fat (Yildiz et al. Citation1998; Sanmee et al. Citation2003). For populations that do not eat animal proteins (either because of unavailability or religious belief), mushrooms are utilized to regulate protein deficiency and to complement cereal grains. Protein found in mushrooms contains all nine essential amino acids (EAAs) as opposed to the most other plant-based protein sources that usually lack one or two EAAs. In fact, mushrooms possess a high branched-chain amino acid (BCAA) composition, typically present only in animal-based protein sources (DFH Team Citation2019).

Mushrooms have a higher grade of protein content than grains but comparable with other non-animal sources of protein (Porres et al. Citation2002). Mushrooms also contain a range of different types of non-digestible carbohydrates, including β-glucans, chitin, oligosaccharides, raffinose, and resistant starch (Manzi et al. Citation2001; Dikeman et al. Citation2005). The nutritional composition of the widely cultivated mushrooms (Food data central Citation2019) is given in .

Table 1. Nutritional composition of widely cultivated mushroom species.

Han et al. (Citation2016) examined the peculiar qualities of the powder extracted from Pleurotus sajor-caju (PSC) (oyster mushroom) and their results showed that PSC powder had a great content of carbohydrate (60.47 g/100 g), resulting in 451.60 cal/g calorie. Samsudin and Abdullah Citation2019 investigated that mushrooms give both digestible carbohydrates (i.e. mannitol, trehalose, glycogen, and glucose) and non-digestible carbohydrates (i.e. chitin, mannans, and β-glucan). Saiqa et al. (Citation2008) analyzed the mineral composition of Agaricus bitorquis and Agaricus bisporus and identified that they are enriched with essential minerals such as sodium (Na), potassium (K) and lithium (Li), while low in concentration of copper (Cu), chromium (Cr), zinc (Zn), lead (Pb), cobalt (Co), nickel (Ni), and manganese (Mn). They also detected that both mushrooms exhibit high quantities of protein, lipids, and carbohydrates. Ganoderma lucidum, Inonotus obliquus, Lentinus edodes, Schizophyllum commune, Trametes versicolor, Phellinus linteus, Flammulina velutipes, Grifola frondosa, and Cordyceps sinensis possess cancer inhibitory effects and their immune ceuticals act mainly by increasing the immune system of the host. This process involves the activation of dendritic cells, NK cells, T-cells and macrophages, and the production of cytokines (Wasser Citation2010). Hetland et al. (Citation2011) found that Agaricus blazei is plentiful in the immunomodulating polysaccharides, β-glucans, and has been disclosed to have anti-infection, antitumor, and antiallergic/-asthmatic properties in mouse models, conjoined with anti-inflammatory impact in inflammatory bowel disease patients. These impacts are due to the mushroom’s stimulus of innate immune cells, such as monocytes, NK cells, and dendritic cells, and the enhancement of a skewed Th1/Th2 balance and inflammation. Mushrooms have been identified as therapeutic foods that are useful for the prevention of diseases such as hypercholesterolemia, hypertension, and cancer (Bobek et al. Citation1995; Bobek and Galbavý Citation1999). These properties of mushrooms are primarily due to the presence of dietary fiber and especially because of chitin and beta-glucans (Manzi et al. Citation2001). A daily intake of mushrooms can boost the human body’s immune responses, thereby enhancing the disease tolerance and causing reversion of an ailment (Chang and Buswell Citation2008). The therapeutic and nutritional attributes of mushrooms help to fight against the pandemic Covid-19 as they boost the immune system and countermeasures the superinfection associated with the Covid-19 attack (Hetland et al. Citation2020). As the number of wild mushrooms decreases due to environmental deterioration and destruction of habitat, the cultivated mushrooms will provide not only food security but also a healthier and balanced diet (Vinceti et al. Citation2013).

The present study summarizes that the population of the world is facing the malnutrition problem and this grave issue of malnutrition can be addressed through the superfood like a mushroom. Nowadays the importance of mushrooms has been increased more when everyone is susceptible to the pandemic coronavirus and the only way to fight is to boost the immune system which could be possible by the intake of healthy produce such as mushrooms. But there is a need to develop awareness among people regarding mushrooms as most of our people are uneducated and unaware of the nutritional and pharmaceutical aspects of mushroom. However, it is the vast untapped source of food in the world and can reduce the problems of health and malnutrition.

Food security assurance

Food is one of the essential needs of life. It gives the energy to perform all necessary activities of life. Food security exists when ‘all people, have physical, economic and social access, at all times, to safe, sufficient, and nutritious food that fulfills their dietetic requirements and food preferences for a healthy and active life’ (WHO Citation2012) and the four main pillars of food security are availability, access, usage, and stability (CFS Citation2011). With the proper awareness among people regarding the nutritional, pharmaceutical, and economical peculiarities of mushrooms and by their cultivation at the industrial and cottage scale, mushrooms can meet all the fundamentals of food security. Humanity has been dealing with hunger and food shortages for years as various determinants leading to low agricultural production. Increasing population, desertification, and urbanization making this situation more severe. This problem is quite high in African countries and developing Asian countries (Pandey et al. Citation2018). In 2009, Chief Scientific Advisor of the UK Government, Professor John Beddington, cautioned that increasing populations, declining energy reserves, and food deficiency would create a ‘perfect storm’ of food, water and energy scarcity by 2030 (The Guardian Citation2009; The Guardian Citation2011). In 2019, approximately 750 million (1 of every tenth individual of the world) were exposed to severe levels of food insecurity (Sustainable Development Goals Citation2020).

The ever-rising human demand for protein-rich food and the incompetence of traditional methods have developed the need to scrutinize alternatives for cheap and unconventional protein-rich food production (Mukherjee and Nandi Citation2004). One of the best alternatives is edible fungi or mushrooms belonging to the Basidiomycetes. Mushroom being an indoor crop, using vertical space provides a way to shrink land and greater waste utilization, and recognized as the biggest protein producer per unit area and time nearly 100 times higher than typical agriculture practice. (Singh et al. Citation2011). Mushrooms are a superfood and one of the world’s healthiest foods, approximately 50% of edible mushrooms are recognized functional food meaning that over and beyond basic nutrition, they have a potentially beneficial health impact (Food Revolution Network Citation2016). The Chinese have identified 966 edible mushrooms and 576 therapeutic types of which, nearly 70 species can be cultivated and 18 species can be cultivated industrially (Dai et al. Citation2009). Up to now, the mushroom industry is an industry with world production larger than 25 million tons. China is the current largest mushroom producer in the world and has achieved more than 20 million tons that account for over 80% of the world's mushroom production (Li Citation2012).

Today mushroom farming is being carried out in more than 100 countries and its production is growing at 6–7% annually. In some developed European and American countries, mushroom farming has secured the status of a high-tech industry with a high degree of mechanization and automation (Singh et al. Citation2011). The Asia Pacific is the leading region in the global mushroom production market. . showing the region-wise production rate of mushroom and truffles (FAO Citation2018). China, which is the largest producer of mushrooms in the world, has a higher per capita consumption than any other country.

Figure 1. Region wise production of mushrooms and truffles.

Figure 1. Region wise production of mushrooms and truffles.

China beats the world in the production of Lentinula edodes, Volvariella volvacea, Agaricus bisporus, Wolfiporia cocos, Tremella fuciformis, Auricularia auricula-judae, Auricularia polytricha, Pleurotus ostreatus, Flammulina velutipes, Pleurotus eryngii, and Hericium erinaceus (Wu et al. Citation2013). Most mushroom consumption in China, EU and India was provided from domestic sources; and almost all mushroom consumption in the United States, Japan, Australia and Canada was supplied primarily by domestic sources but also by large quantities of imports (USITC Citation2010).

African people are suffering from the insufficiency of food and malnutrition problems for decades and the main reason is the uptake of staple foods with low micronutrients and protein contents that developed the need for the production of home-based protein enriched food such as mushrooms that can compete for the protein and mineral deficiency among people of developing and under-developing countries as the unconventional food fortification strategy (Ishara et al. Citation2018).

A good example of the attainment of food security by mushrooms comes from Nigeria where people look towards the mushroom and their production to fight poverty, hunger and malnutrition (The Guardian Citation2018). Now, the People of Bamenda Highlands also look towards mushrooms in the food shortage period for food security assurance (Fongnzossie et al. Citation2020)

The three International forums/bodies were established to uplift the mushroom industry all over the world: (i) The international movement for edible mushrooms, (ii) The international movement for medicinal mushrooms, and (iii) The international movement for wild mushrooms, primarily concerned with edible mycorrhizal mushrooms (Chang Citation2006). In the global mushroom market, some of the key players include Monterey Mushrooms, Inc. Weikfield Foods Pvt. Ltd. Nasza Chata Ecolink Baltic, Monaghan Mushrooms, BioFungi GmbH, Bonduelle, Scelta Mushrooms BV, California Mushroom Farms Inc., and Agro Dutch Industries Ltd. (Fortune Business Insights Citation2019). This research summarizes that hunger is expanding day by day due to the non-availability of nutritious food at affordable prices to the growing population of the world. Poor agricultural practices and shortage of land further increase the starvation problem but therapeutic and palatable mushrooms cultivation is the best solution to tackle the issue of food insecurity especially in developing and under-developing nations. The major problems for mushroom production and fluctuation in the developing nations are the pathogenic problems, the problems of capital Politics, Corruption, Misuse of Funds, and the weak policies of the government. It is the requirement of today’s world to resolve these issues to get access to the cheapest, nutritious, and tasty food.

The efficient way of agro-industrial waste disposal and zero-emission strategy for food production

Asia is one of the world’s most agriculturally-intensive areas, with 46.9% of crop residue emissions from 2010 to 2016, compared to 28.2% and 16.2% from America and Europe, respectively (Faostat Citation2017). According to the emissions database of Faostat Citation2017, 90.6% of rice grown within Asia generated over one hundred million tons of residual material. This agricultural waste accounted for more than 50% of the nitrous oxide produced from the disintegration of crop leftover on cultivated soils, one of the major sources of the greenhouse gas effect and a reason for global warming. Saprophytic mushrooms especially those that grow on the waste of agricultural origin can turn these lignocellulosic residues into the value-added products such as medicine, food, feed fuel, fertilizer, and recycle the wastes materials (Lowe et al. Citation2012).

shows the commercially cultivated mushroom species use different types of agricultural wastes as the growing medium and convert these residues into the proteinaceous rich food.

Table 2. Different types of agricultural wastes used as the substrate by the commercially cultivated species.

Different value-added products that are produced through solid-state fermentation (SSF) of agricultural residues include mushrooms, animal feed enriched with microbial biomass, compost to be utilized as biofertilizer or biopesticide, enzymes, organic acids, ethanol, flavours, biologically active secondary metabolites for bioremediation of hazardous compounds, and biological detoxification of agro-industrial wastes, biopulping, etc. (Pandey et al. Citation2000; Sánchez et al. Citation2002; Howard et al. Citation2003; Tengerdy and Szakacs Citation2003; Kim and Dale Citation2004; Manpreet et al. Citation2005; Zervakis et al. Citation2005). Among SSF applications, mushroom cultivation has proved its economic strength and environmental significance for the efficient usage, value-addition and bioconversion of agro-industrial residues (Chang Citation1999, Citation2001, Citation2006; Chiu and Moore Citation2001; Zervakis and Philippoussis Citation2000). The hydrolytic disintegration of cellulose is catalyzed by extracellular endoglucanases cellobiohydrolases, and glucosidases present in fungi, that breakdown the long chains of cellulose, releasing cellobiose and finally glucose, while the primary hemicellulose-degrading enzymes are endomannanases and endoxylanases (Tengerdy and Szakacs Citation2003). Some of these enzymes have been discovered in both wood-degrading macrofungi (WDF) (Elisashvili et al. Citation2008) and litter-decomposing macrofungi (LDF) (Steffen et al. Citation2007).

Lignin breakdown is because of the lignin peroxidase (LiP), manganese peroxidase (MnP), and laccase (Hatakka Citation1994). MnP is secreted by nearly all wood-degrading basidiomycetes (Steffen et al. Citation2007). Other than the lignocellulosic enzyme complex, lignocellulolytic fungi also release other enzymes, such as proteases, pectinases, proteases, and lipases on lignocellulosic substrates (Tengerdy and Szakacs Citation2003). Téllez-Téllez and Diaz-Godinez (Citation2019) identified that Pleurotus genus release various enzymes, including laccases, versatile peroxidases, manganese peroxidases, peptidases, glycosyl hydrolases, peptidases, and esterases/lipases that promote the mineralization proceedings. Depending upon the habitats and ecological niche, saprophytic mushrooms exude a high number of hydrolases encoded with multigene families to feed on complicated molecules in the environment (Lowe et al. Citation2012).

About 1 kg of mushroom production will produce 5 kg of spent residual material called spent mushroom substratum (SMS) (Lau et al. Citation2003). An ordinary farm disposes of more than 24 t of SMS per month. After the final crop harvest, the spent mushroom substratum (SMS) still has several positive attributes left for its promising utilization (Singh et al. Citation2011). The material has been discovered to be a rich source of nutrients for horticultural and field crops. Along with this, it exhibits immense cation exchangeability and has a low mineralization rate that maintains its quality as an organic matter. Mushrooms through bioconversion processes reutilize the spent substrates and convert the polluting material into valuable food products (Beyer Citation2005; Noble Citation2005). They can accumulate and filter pollutants and act as one of the most promising and effective bio sorbents of toxic heavy metals from radioactive nuclear fallout polluting water and soil, thereby acting as neutralizers of pollutants (Das Citation2005).

Singh et al. (Citation2010) found eight dyes (tryphan blue, remazol brilliant blue R, amido black, bromophenol blue, methyl green, crystal violet, methylene blue and congo red) decolourised by lignin peroxidase extracted from 5-month-old SMS of Pleurotus sajor-caju conjoined with veratryl alcohol as a redox mediator. Kim et al. (Citation2011), worked on spent A. bisporus substrates and reported that the protein contents increased and fiber contents decreased in the substrates due to the mycelial activity during the A. bisporus cultivation process showed that it could be utilized as a potential food source for ruminants. This research finds that mushroom farming is the most efficient way of agro-industrial disposal and convert these residues into the mushroom substrate to grow mushrooms and its spent mushroom substrate has further various application to make it zero-emission strategy for food production but advanced research is needed to understand the enzyme degradation capacities of mushrooms to get maximum benefits from this microbial technology.

Economic intensification through mushroom farming

Beverages and food from fungi is a business of multi-million dollar and wild mushrooms are an indispensable way of income for numerous poor societies and of worth to competitive foragers, and especially in Asia, most of the development has been consolidated on mushrooms due to their nutritious qualities and medicinal significance (Hyde et al. Citation2019; Li et al. Citation2021). The global market for the mushroom industry in 2005 was valued at over $45 billion (Chang Citation2006) while in 2013 was valued at nearly $63 billion, the world market for edible mushrooms continues to rise from US$ 34.1 billion in 2015 to US$ 69.3 billion by the end of 2024 due to the nutritional, culinary and health benefits of mushrooms (Valverde et al. Citation2015; Bal et al. Citation2018). Cultivated, edible mushrooms are the main component (54%) responsible for approximately $34 billion, while medicinal and wild mushrooms account for $24 billion (38%) and $5 billion (8%) of the total respectively (Zied and Pardo-Giménez Citation2017). The consumption of mushrooms increased on a global scale from 1 to 4.7 kg of cultivated edible mushrooms per capita between 1997 and 2013 (Royse et al. Citation2017). Global market consumption in 2018 was 12.74 million tons and is expected to hit 20.84 million tons by 2026, with a forecast CAGR (Compound Annual Growth Rate) of 6.41% (Fortune Business Insights Citation2019). Cultivation of mushrooms can help decrease susceptibility to poverty and improve livelihoods by producing a fast yielding and nutritious food source and a stable source of income. Since mushroom cultivation does not require access to land, it is a practicable and appealing activity for both rural farmers and peri-urban residents. Small-scale production does not need any large capital investment as mushroom substrate can be prepared from any clean agricultural residue material, and can be grown in temporary clean shelters. They require little maintenance and can be cultivated as a part-time activity (Marshall and Nair Citation2009). Hang et al. (Citation2008) described that mushroom cultivation is labor-intensive agriculture, it creates great job opportunities. It was estimated that nearly 25 million individuals pursue the mushroom cultivation and preparing industry. A great example of the mushroom cultivation to adopt as the income source comes from the Kilimanjaro highlands Tanzania that was once a thriving banana and coffee-growing region, but with falling world market prices for coffee and unreliable rain in the lowlands, farmers have struggled to earn an income and produce enough food. Later on, farmers were progressively convinced of the value of growing and consuming oyster mushrooms. The benefits of growing and selling mushrooms have allowed farmers to purchase livestock (chickens and goats), pay school fees and household goods, and now a number of farmers have invested in increasing their production of mushrooms (New Agriculturalist Citation2007). Mushroom farming is practiced in many parts of the world and their production continues to rise to ease the pressure on the natural resources and economic intensification (Grimm and Wösten Citation2018 Wendiro et al. Citation2019;).

Based on the latest statistic report from the Food and Agriculture Organization of the United Nations, in 2018 China (contributed almost 77% of world production), the United States, the Netherlands, Poland, and Spain were reported as the top five mushroom and truffle producers in the world as shown in the .

Table 3. Leading producer countries of mushrooms and truffles (Source: Faostat Production database, 2018).

The current findings show that the mushroom production not only increases the income source at the local level but its commercial and industrial farming enhances the foreign exchange also that can strengthen the economy of any country.

Conclusion

In the modern world, wild mushrooms and mushroom farming is the only way to ensure food security and to combat malnutrition without affecting the environment, it is a step towards a non-green revolution. Reliance on the green part of nature for fiber and proteins can be reduced through practicing mushroom cultivation at the large scale. It is the best source to achieve zero hunger and no poverty sustainable development goals of the United Nations. Developing countries are facing a lot of crises including poverty, malnutrition, unemployment, food insecurity, and pollution but by adopting mushroom cultivation as a welcoming industry in these countries these above-mentioned problems can be solved. A further detailed study is needed regarding the therapeutic and biotechnological applications of mushrooms to take maximum advantages of this vast untapped source of food on earth.

Acknowledgement

The authors are highly acknowledged to Dr Nida Ahsan (Assistant Professor, Department of English, University of the Punjab, Lahore) for her linguistic check to improve the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

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