Abstract
The environmentally acceptable disposal of agricultural wastes and residues constitutes a major scientific challenge, especially when their chemical properties, recalcitrance, and abundance are taken into account. The use of macrofungi, which grow in nature as wood or litter decomposers and excrete nonspecific oxidative enzymes to degrade lignocellulosics, seems to offer solutions that could be widely and readily applied for the biotransformation of such materials. More importantly still, these organisms demonstrate efficient bioconversion of various types of agro-industrial/forestry by-products with low or no economic value to edible biomass. The process involves controlled solid-state fermentation which is optimized for the production of culinary and medicinal mushrooms, thus providing food of high organoleptic and dietetic value. In addition, their content in bioactive compounds related with anticarcinogenic, antidiabetic, antihypertensive, anti-inflammatory, immunostimulating, and other health-beneficial properties has repeatedly been demonstrated. In this chapter, the enzymatic mechanisms behind lignocellulose degradation by fungi are summarized, and several of the most important cultivated mushrooms are presented with respect to their production requirements and medicinal properties.
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1 Introduction
Kingdom Fungi comprises eukaryotic, heterotrophic microorganisms with absorptive nutrition. They secrete oxidative exoenzymes to degrade their growth substrates, and nutrients are absorbed in soluble form by an extended network of branched hyphae (thread-like tubular structures demonstrating apical growth) which form the mycelium. Fungi demonstrate a large variety of life cycles, modes of sexual/asexual reproduction, and ecological preferences.
At present, ca. 100,000 fungal species are recorded and account for no more than 7% of the estimated total of 1.5 M species (Hawksworth 2001). The phylum Basidiomycota comprises about one-third of all described fungi (Stajich et al. 2009); more particularly, Agaricomycotina constitutes a diverse clade including 20,000 species (Hibbett 2006), the great majority of which could be described as macrofungi. This term is widely used for fungi forming macroscopically visible reproductive structures (i.e., organs where spores are formed and liberated from) or mushrooms. Although most macrofungi are classified in Basidiomycota, some belong to the phylum Ascomycota.
The larger part of macrofungi exhibits a saprotrophic lifestyle (as opposed to those demonstrating symbiotic or parasitic ecological preferences), which means that they rely on decomposing animal and plant residues for obtaining nutrients. Therefore, these particular organisms constitute the major agents of degradation and recycling of dead organic matter in nature. The ability of such wood- and litter-decaying microorganisms in converting complex lignocellulosics (the basic structural material of plant cell walls) into simple organic compounds has been widely exploited in numerous biotechnological applications (Harms et al. 2011).
2 The Enzymatic Arsenal of Macrofungi in the Degradation of Lignocellulosics and Related Organic Compounds
Huge quantities of lignocellulosics are produced every year in nature; it is estimated that the quantity of terrestrial biomass generated annually is 200 × 1012 kg (Foust et al. 2008). Lignocellulosics are particularly resistant to microbial degradation because of the complex structure by which polymers of cellulose, hemicellulose, and lignin are bound together. Cellulose forms straight and tightly packed chains of microfibrils composed of β-d-glucose units and linked by H-bonds, whereas hemicelluloses are arranged around the rigid cellulose core, and they consist of various pentoses and hexoses (e.g. xylan, arabinose, glucomannan). In plant cell walls, both cellulose and hemicelluloses are surrounded by a layer of lignin which is particularly recalcitrant due to the existence of three aromatic alcohols known as monolignols (i.e., p-coumaryl alcohol, coniferyl alcohol, and sinapyl alcohol) forming the phenylpropanoid p-hydroxyphenyl, guaiacyl, and syringyl units linked by ether and carbon to carbon bonds (Camarero et al. 2014).
As previously stated, saprotrophic basidiomycetes are among the primary factors of decomposition and recycling of plant debris in nature, and hence they rely heavily on the production of cellulolytic and ligninolytic enzymes for degrading their growth substrates. The former category of enzymes includes endoglucanases and exocellulases (cellobiohydrolases), which decompose cellulose to cellobiose or cello-oligosaccharides that are further processed by β-glucosidases or by cellobiose dehydrogenase. Endo-1,4-β-glucanase (EC 3.2.1.4, endocellulase) is common among Basidiomycota, notably in both white and brown rot fungi and in litter-decomposing species (Cohen et al. 2005; Martinez et al. 2009; Steffen et al. 2007). Multiple endoglucanases are generated by fungi; they are monomeric structures, which demonstrate catalytic optima at pH 4.0–5.0, and their activity is mainly oriented toward amorphous regions in the cellulose molecule (Baldrian and Valášková 2008). Cellobiohydrolase (CBH, EC 3.2.1.91; exocellulase) is mainly present in white-rot and litter-decomposing fungi and is typically active on crystalline cellulose, Avicel (Baldrian and Valášková 2008; Rytioja et al. 2014). On the other hand, β-glucosidase (EC 3.2.1.21) is produced by numerous macrofungi and demonstrates high structural variability; it is relatively nonspecific (it cleaves other simple carbohydrates as well), and although it usually attacks cello-oligosaccharides, it is inactive on crystalline cellulose and shows low activity on amorphous cellulose (Baldrian and Valášková 2008). Last, cellobiose dehydrogenase (CDH; EC 1.1.99.18) is a typical oxidoreductase which oxidizes cellobiose and higher cellodextrins by employing a wide range of electron acceptors including quinones, phenoxyradicals, cytochrome c, etc. (Zamocky et al. 2006). CDH is produced mainly by white-rot fungi under cellulolytic conditions together with cellulases and hemicellulases; although it binds specifically to cellulose, it could also degrade hemicelluloses and lignin in the presence of iron and hydrogen peroxide (Henriksson et al. 1997).
The ligninolytic enzymes are mainly produced by wood-rot (notably white-rot) fungi and some related litter-decomposing basidiomycetes which demonstrate efficient lignin degradation (Hatakka 2001). These enzymes are largely nonspecific and include phenol oxidases (laccase), heme peroxidases (i.e., lignin peroxidase, manganese peroxidase, and versatile peroxidase), as well as several other accessory enzymes (e.g., veratryl alcohol oxidase and glyoxal oxidase), which oxidize the heterogeneous polymeric substrates through multistep electron transfers accompanied by the formation of intermediate cation radicals (Hatakka and Hammel 2011). In particular, lignin peroxidases (LiPs, EC 1.11.1.14) catalyze the oxidation of non-phenolic lignin substructures (in the presence of hydrogen peroxide) to produce aryl cation radicals, which are further degraded/mineralized by nonenzymatic means (Kirk and Farrell 1987). Manganese peroxidase (MnP, EC 1.11.1.13) oxidizes bivalent Mn (Mn2+) to trivalent Mn (Mn3+) and the latter catalyzes the oxidation of phenolic lignin moieties leading to their decomposition (Gold et al. 2000). Laccases (Lac, EC 1.10.3.2) are multicopper oxidases catalyzing the conversion of phenolic rings to phenoxy radicals in a reaction without the presence of H2O2 (Baldrian 2006). In addition, versatile peroxidase (VP, EC 1.11.1.16) can oxidize aromatic compounds and Mn2+, while its catalytic mechanism is similar to LiP; VPs have been detected in a few macrofungi, including species of Bjerkandera and Pleurotus (Ruiz-Dueñas and Martínez 2009). Last, the H2O2 needed for supporting oxidative reactions during ligninolysis in the presence of LiP and MnP is provided through the action of extracellular oxidases. As such, glyoxal oxidase (GLOX) and aryl alcohol oxidases (AAOs) reduce O2 to H2O2 by oxidizing the co-substrates (Hammel et al. 1994).
3 Mushroom Cultivation on Lignocellulosic Residues and Agro-industrial By-Products
A vast amount of plant residues and agro-industrial by-products remains largely unexploited. Only in the European Union, more than 80 million tons of wheat straw and corn cobs are produced annually (data from http://faostat.fao.org, and http://www.indexmundi.com/agriculture), in addition to several other by-products of similar origin, e.g., various grasses, leaves, tree pruning, wood bark and sawdust, cotton gin trash, almond, chestnut and walnut shells, grape marc, olive mill waste, etc. The composition of many such materials, which are rich in lignocellulosics and are already in use or demonstrate a promising potential to be used as growth substrates for macrofungi, is presented in Table 12.1.
Cultivation of mushrooms constitutes a noteworthy case of sustainable exploitation of various lignocellulosics through a controlled solid-state fermentation process which converts them to edible biomass. Such bioconversions are based on well-established methodologies involving discrete phases of substrate preparation (including wetting, mixing, and, often, composting of ingredients), pasteurization, spawning, incubation (spawn run), and mushroom induction, production, and harvest. Optimal environmental conditions for fruit-body primordia formation, minimum crop length, maximum yields, and product quality are under continuous investigation as is the selection of most suitable substrates for each species.
Currently, the global mushroom production is estimated at about 27 million tons presenting a 25-fold increase during the last 40 years (Royse 2014); it is estimated that ca. two-thirds of this quantity originates from China. In parallel, per capita consumption of mushrooms has quadrupled from 1997, exceeding nowadays 4 kg per person. Five fungal genera represent 85% of the world’s total mushroom production (Royse 2014), i.e., Agaricus (mainly A. bisporus and substantially lower quantities of A. brasiliensis) with almost one-third of totally cultivated mushrooms, Pleurotus (principally P. ostreatus, but also P. eryngii, P. pulmonarius, P. citrinopileatus, and P. djamor) with about 27%, and Lentinula edodes at ca. 17% of the world’s output. Auricularia and Flammulina rank fourth and fifth with 6% and 5% of the total volume, respectively. Other cultivated mushroom species with notable medicinal properties are Ganoderma lucidum and Trametes versicolor, while Pholiota nameko, Hericium erinaceus, Grifola frondosa, Tremella fuciformis, Volvariella volvacea, and Cyclocybe cylindracea are popular edible species in many regions of the world.
In general, mushrooms are a high-protein and low-calorie food which also contains metals, vitamins, and important bioactive compounds. Their water content is high (commonly ranging from 86 to 92%), while their average content in total proteins, total fats, and ash are 250, 30, and 80 g kg−1 dry matter, respectively; the rest is mainly composed of various carbohydrates (Kalač 2013). In the protein fraction, the most abundant amino acids are glutamic acid (13–21%), aspartic acid (9–12%), and arginine (4–12%); they also contain tyrosine, leucine, lysine valine, and alanine (usually more than 1 mg g−1 fresh weight) (Manzi et al. 1999; Mattila et al. 2002a, b). As concerns their content in lipids, more than ten fatty acids are found in cultivated mushrooms; linoleic, oleic, and palmitic acid are the most representative. Moreover, polyunsaturated fatty acids in cultivated mushrooms exceed 70% of the total (Reis et al. 2012). Mannitol and trehalose are the most common among alcoholic sugars and oligosaccharides, respectively, and β-glucan is the most common and well-known fungal polysaccharide (Kalač 2013; Reis et al. 2012). Potassium is highly accumulated by mushrooms followed by calcium and sodium, while mushrooms also contain significant amounts of zinc and copper when compared to other foods (Kalač 2013; Koutrotsios et al. 2014; Mattila et al. 2001). Trace element content in mushrooms varies greatly among different species, but it also depends on their concentration in the growth substrate. As far as vitamins are concerned, ascorbic acid (vitamin C) content varies from 150 to 300 mg kg−1; thiamine (B1), riboflavin (B2), niacin (B3), and pyridoxine (B6) contents are 1.7–6.3, 2.6–9.0, 63.8–83.7, and 1.4–5.6 mg kg−1 respectively, and ergosterol (a provitamin to D2) varies from 3 to 7 g kg−1 dry matter (Kalač 2013).
4 Widely Cultivated Species: Mushroom Production and Their Bioactive Compounds and Medicinal Properties
Among the most interesting (in terms of their content in mushrooms and their effect on various functions of the human body) and well-known bioactive compounds produced by cultivated mushrooms are ergothioneine, phenolics, and triterpenoids (all potent antioxidants), β-glucans with anticancer and prebiotic activities, γ-aminobutyric acid (i.e., the chief inhibitory neurotransmitter in the mammalian central nervous system), and lovastatin with hypocholesterolemic and hypolipidemic properties. An overview of pertinent literature findings is presented in Table 12.2. Moreover, a brief outline of available information for each of the most important cultivated mushroom species is provided below.
4.1 Agaricus spp.
Agaricus species include litter-decomposing saprotrophs able to efficiently degrade all components of the lignocellulosic complex. They grow in humus-rich soils and are often found in places used for animal grazing. A. bisporus (also known as button mushroom or champignon) in particular has been an important component of human diet for over 200 years, and its worldwide cultivation constitutes a multibillion-dollar industry (Fig. 12.1a). In commercial cultivation, most production substrates are typically composed of wheat straw (in Europe and the USA) or rice straw (in Asia) with chicken or horse manures which are mixed and subjected to a composting process. Moreover, an organic material (casing layer) consisting mainly of peat moss is applied over the colonized by the Agaricus mycelium substrate for promoting the initiation and development of fruit bodies (Gülser and Pekşen 2003). Since in many areas horse manure and peat moss are scarce and/or expensive, many efforts have been made to develop alternative inputs for use in substrates or casing layers, e.g., wheat bran, molasses, pigeon manure, coconut fibers, straws from oat and grass, spent mushroom compost, residues from tea cultivation, and olive mill waste (Baysal et al. 2007; Giménez and Pardo-González 2008; Gülser and Pekşen 2003; Yigitbasi et al. 2007).
Agaricus brasiliensis (the names A. subrufescens or A. blazei being also in use for this species) is a mushroom recently discovered (1945) in Brazil, but its popularity is increasing rapidly, especially among Brazilian, Japanese, and Chinese growers. In general, its requirements in infrastructure are similar to those for the cultivation of A. bisporus, but formation and maturation of mushrooms are achieved at a higher temperature (22–25 °C vs. 15–18 °C respectively). Therefore, A. brasiliensis has the potential to replace the cultivation of A. bisporus in the warm summer months when the temperature rises above the optimal range for the latter. Its commercial substrate consists of rice straw or bagasse supplemented with chemical and organic fertilizers (Iwade and Mizuno 1997). However, the suitability of various other materials was also evaluated, e.g., sugarcane, coast cross grass and soybean meal, asparagus straw, and sunflower seed hull-based compost (Matute et al. 2010).
A. bisporus mushrooms contain significant amounts of lectins with potent antiproliferative effects on human epithelial cancer cells (Batterbury et al. 2002), antioxidants such as selenium and polyphenols, and vitamins (Koyyalamudi et al. 2009). On the other hand, A. brasiliensis contains a higher amount of β-glucans and proteoglycans in comparison to A. bisporus (Ohno et al. 2001), while it also produces agaritine and ergosterol which induce apoptosis of leukemic cells, as well as isoflavonoids with hypoglycemic properties (Oh et al. 2010). Furthermore, compounds from this fungus were demonstrated to possess antitumor properties against fibrosarcoma, myeloma, ovarian and lung cancer in experiments with animals, and gynecological cancer and leukemia (Hetland et al. 2008).
4.2 Pleurotus spp.
Pleurotus species (known as “oyster mushrooms”) are distributed worldwide and grow on a very large range of substrates (mostly hardwoods). They are potent white-rot fungi with the ability to colonize and form fruit bodies on various lignocellulosic residues; this in combination with the relative ease of cultivation and their culinary/nutritional value are the main reasons for the significant increase in their commercial production during the last 20–30 years. Especially as regards P. ostreatus (Fig. 12.1b), the most commonly cultivated species of this genus, a wide variety of available strains are available, with different requirements with respect to climatic conditions and/or mushroom appearance and quality (Koutrotsios et al. 2017), including sporeless strains especially developed to overcome the problems often observed on people working in cultivation rooms due to the large production of spores. The substrates mostly used are composed of cereal straw supplemented with wheat, rice, or soy bran and/or flours from various leguminous seeds aiming at reducing the cultivation period and/or at increasing mushroom yields. Of interest is that many other plant residues and agro-industrial by-products were exploited for Pleurotus cultivation, e.g., sawdust, wood chips, cottonseed hulls, corn cobs, sugarcane bagasse, cotton gin trash, coffee husks, grape marc, vineyard pruning, olive mill wastes, banana straw, soybean stalk, waste paper, and nut shells (Das and Mukherjee 2007; Koutrotsios et al. 2014; Mandeel et al. 2005; Membrillo et al. 2011; Obodai et al. 2003; Pant et al. 2006; Philippoussis et al. 2001; Salmones et al. 2005; Sánchez et al. 2002; Yildiz et al. 2002; Zervakis et al. 1996, 2013). Substrates are usually pasteurized, spawned, and then placed in blocks or bags of 10–20 kg. Biological efficiency (BE, i.e., percentage ratio of fresh mushroom weight over the dry weight of the substrate) differs considerably by ranging from 4 to 74% in various types of sawdust, from 50 to 97% in straw-based substrates, or up to 139% in grape marc, vineyard pruning, and cotton residues (Fig. 12.2a) (Koutrotsios et al. 2014; Mandeel et al. 2005; Pant et al. 2006; Philippoussis et al. 2001; Salmones et al. 2005; Sánchez et al. 2002). Other species, such as P. eryngii (Fig. 12.1c), P. pulmonarius, P. citrinopileatus (Fig. 12.1d), and P. djamor, although producing mushrooms of different appearance, taste, and composition, have rather similar requirements in infrastructure, substrate, and growth conditions.
Mushrooms and mycelium of Pleurotus spp. contain bioactive compounds such as polysaccharides, lectins, peptides, triterpenoids, etc. with a plethora of medicinal properties including antitumor, anti-inflammatory, and immunomodulatory activities. Among polysaccharides, a β-glucan (pleuran) was identified with antioxidant and anti-inflammatory properties (Bobovčák et al. 2010). Furthermore, trials on humans demonstrated the efficacy of pleuran in the prevention of recurrent respiratory tract infections (Jesenaket al. 2013). Preliminary results also showed that addition of Pleurotus mushroom powder in animal diet (at a rate of 4–10%) resulted in lower blood pressure as well as cholesterol levels (Pate et al. 2012). Moreover, when compared to all other cultivated mushrooms, P. ostreatus contains the highest concentration of lovastatin and ergothioneine (up to 980 mg/kg and 944–2444 mg/kg respectively; Table 12.2).
4.3 Lentinula edodes
Lentinula edodes (commonly known as “shiitake”) grows on dead wood of various deciduous trees in warm and moist regions (Royse 1997; Royse and Sanchez-Vazquez 2001). This is the first mushroom ever cultivated in China 1000 years ago, by placing (in woods) cut logs naturally contaminated by the fungus. Nowadays, it is cultivated in artificial substrates in Asia, Europe, and North America and ranks third in global production because of its flavor, taste, and nutritional and medicinal value (Özçelik and Pekşen 2007). During the last 20 years, the traditional cultivation technique on wood logs has been largely replaced by production on artificial substrates typically consisting of hardwood sawdust supplemented with various nitrogen sources (Özçelik and Pekşen 2007; Philippoussis et al. 2003, 2007; Royse 1997) (Fig. 12.3); these new techniques offer much higher yields in shorter crop periods (Royse 1997). In addition, several plant residues such as wheat straw, corn cobs, sugarcane bagasse, sugarcane leaves, coffee husks, sunflower seed hulls, peanut shells, cotton stalks, hazelnut husks, tea waste, and vineyard pruning were also used for cultivation of shiitake, supplemented with wheat or rice bran, millet, rye, and/or corn in a 10–40% ratio to the main ingredient (Curvetto et al. 2002a, b; Elisashvili et al. 2008; Gaitán-Hernández et al. 2006; Hiromoto 1991; Mata and Savoie 1998; Royse and Sanchez 2007; Salmones et al. 1999). Biological efficiencies ranged from 60 to 65% in hardwood residues and hazelnut husks to 79–89% for cereal straw and sugarcane bagasse and up to 93–108% in vineyard pruning and sunflower seed hulls (Fig. 12.2b) (Curvetto et al. 2002a, b; Gaitán-Hernández et al. 2006; Hiromoto 1991; Özçelik and Pekşen 2007; Salmones et al. 1999). The particular aspect of shiitake cultivation is that the crop requires an extra stage (which extends the length of cultivation) just after the substrate’s full colonization by the mycelium; this is known as “browning” since mycelium turns from white to brown and a hard crust of hyphae forms on the surface of the substrate.
Shiitake mushrooms contain several bioactive compounds, i.e., lentinan, lentin, lentinacin or eritadenine, polysaccharide KS-2, and lentinamycin (Enmanet al. 2008; Fujiiet al. 1978; Minato et al. 1999; Shimada et al. 2003), all with interesting medicinal properties. Among them, lentinamycin, lentin, and lentinan (a β-glucan) demonstrate antimicrobial and antiviral activities, lentinan suppresses the proliferation of leukemic cells, ethanol extracts of fruit bodies decrease proliferation of CH72 cells without affecting healthy cells, KS-2 polysaccharides possess properties against Ehrlich and Sarcoma-180 tumors, and eritadenine contributes significantly to the reduction of cholesterol and triglycerides (Casaril et al. 2011; Fujii et al. 1978; Gu and Belury 2005; Handayani et al. 2011; Ngai and Ng 2003). In addition, L. edodes mushrooms contain a significant amount of γ-aminobutyric acid (351–622 mg/kg) and ergosterol (495–1246 mg/kg) (Table 12.2).
4.4 Auricularia spp.
Αuricularia auricula-judae and A. nigricans (also known A. polytricha) are the two most important representatives of the genus. They are saprotrophs with a worldwide distribution from the temperate regions to the tropics, growing on living and dead deciduous trees, decayed stumps, or logs (Du et al. 2011). Nowadays, Auricularia mushrooms are among the top four most important cultivated mushrooms in the world with an annual production exceeding 3.5 million tons (Royse 2014). Their form and the unique jelly texture, as well as the distinctive flavor and nutritional characteristics, make them very different from other cultivated mushrooms (Fig. 12.3b). Their cultivation is rather easy, fruit bodies are produced within a relatively short period, and they do not require expensive facilities (Irawati et al. 2012). In addition, they could be obtained from a wide range of plant residues including cotton seed shells, sawdust, sugarcane bagasse, grass and cereal straw, and corn cobs with BEs reaching 70–80% (Liang et al. 2016; Luo 1993; Onyango et al. 2011). A. nigricans, in particular, is the best-studied species of the genus as regards cultivation on various lignocellulosic substrates. Hence, sawdust supplemented with different quantities of grass plants provided high BE values (95–148%) (Liang et al. 2016); similarly, sawdust, oil palm fond and spent grain, or sawdust with empty fruit bunch supplemented with spent grains performed very well (BE: 261–290%). In contrast, other substrates such as sawdust, supplemented paddy straw, or palm residues were less productive (BE: 6–114%) (Irawati et al. 2012). Although the addition of a nitrogen source is considered a necessary prerequisite for achieving high yields (Luo 1993), the results of pertinent studies show that the optimum C/N value of substrates is about 100 and that further nitrogen addition leads to a reduction in mushroom yields.
A. nigricans and A. auricula-judae are two of the most important medicinal fungi in China. Besides their flavor and nutrition value, they also possess significant antitumor, hypoglycemic, anticoagulant, antiviral, and antimicrobial activities (Wasser and Weis 1999).
4.5 Flammulina velutipes
Flammulina velutipes, commonly known as enoki (“enokitake”) or golden needle mushroom, was first cultivated in China during the eighth century. Nowadays, it ranks fifth among all mushrooms. Recently, its production exceeded 2 million tons, and more than 75% of this quantity originated from China, while Japan, Korea, and Taiwan follow in the leading positions (Royse 2014). Cultivation of F. velutipes is commonly performed in polypropylene bottles which are filled with hardwood sawdust and sterilized prior to inoculation. For the production of high-quality mushrooms, low ambient temperature (3–8 °C) is required, and a plastic collar is placed around the bottle neck to promote the formation of fruit bodies with elongated stipes. Apart of sawdust, several other substrates are in use, e.g., sugarcane bagasse, corn cobs, and cottonseed husks (Chang and Miles 1989; Royse 1997). Moreover, additional plant residues have been evaluated either individually or in combination and presented high biological efficiencies (Fig. 12.2c); indicative examples are paddy straw (BE: 90–106%) (Harith et al. 2014); coffee spent ground (78%) (Leifa et al. 2001); maize straw (73%), rubber wood sawdust with paddy straw, palm empty fruit bunches, and palm press fiber in various proportions (100–185%) (Harith et al. 2014); and wheat straw, sawdust, and wheat bran (265%) (Rezaeian and Pourianfar 2016). As regards the effect of nitrogen supplementation, it was reported that F. velutipes grows well in media containing soybean powder, beef cream, and yeast powder, whereas growth is slowed when nitrates or amines are used as nitrogen sources (DeChang 2000).
Several bioactive compounds have been isolated from fruit bodies and mycelium of F. velutipes, i.e., Fip-FVE protein and enokipodins with proven antimicrobial activity (Ishikawa et al. 2001; Wu et al. 2008), the weakly acidic glycoprotein proflamin with antitumor properties, and the protein flammulin, which is also active against various types of cancer cells (Ikekawa et al. 1985; Gong et al. 1998; Maruyama and Ikekawa 2005). Consumption of enoki mushrooms was demonstrated to reduce the cholesterol level in human body and the allergic immune response in case of food allergies (Hsieh et al. 2003; Ishikawa et al. 2001). In addition, and much like other cultivated mushrooms, it contains antioxidant substances; it is noteworthy that extracts and powder of F. velutipes were used as preservatives against meat and fish oxidation (Bao et al. 2008, 2009).
4.6 Ganoderma lucidum
Ganoderma lucidum, commonly known as lingzhi or reishi mushroom, is one of the most famous medicinal “herbs” in Asian countries which is extensively used since antiquity (Bishop et al. 2015). Due to the increased demand for its fruit bodies and the qualitative/quantitative differences in the chemical composition of wild G. lucidum mushrooms, commercial cultivation has started in the early 1970s, mainly on supplemented hardwood sawdust but also on agricultural residues such as cereal straw, cotton seed husk, corn cobs, and wheat bran (Li et al. 2016; Xia et al. 2003; Zhou et al. 2012) (Fig. 12.3c). However, the use of alternative substrates provided a considerable increase in yields; BEs values of up to 75% was reported when G. lucidum was cultivated on maize straw supplemented with wheat and maize bran, sawdust, and lime, or on soy and soybean curd residues (Ji et al. 2001). In addition, such substrates supported the production of mushrooms with higher polysaccharide content and showed enhanced antimicrobial, antioxidant, and cytotoxic activities in comparison to those obtained on conventional substrates.
G. lucidum fruit bodies and mycelia contain over 400 different bioactive compounds, mainly triterpenoids and polysaccharides and also steroids, sterols, proteins, peptides, and fatty acids (Paterson 2006). Its medicinal properties have been extensively studied, and several hundreds of relevant papers have been published in the last 30 years. Nowadays, the cultivation of G. lucidum on artificial substrates has led to the wide use of reishi mushrooms and its products (80–85% of them derive from fruit bodies) not only as beverages and food additives but also as drugs for the prevention and/or treatment of hepatitis, diabetes, hypertension, nephritis, leukemia, and tumors or as immunoregulating, antiaging, antioxidant, antifatigue, and sleep-regulating agent (Li et al. 2016; Paterson 2006; Zhou et al. 2012).
4.7 Trametes versicolor
Trametes versicolor, also known as Turkey-tail fungus, belongs to the family Polyporaceae. It is a widely distributed fungus whose mushrooms could be found throughout the year mainly on dead wood of deciduous trees (Fig. 12.3d). Although its fruit bodies are not edible because of its hard-flesh texture, it is among the most potent and best-studied medicinal mushrooms. Cultivation of T. versicolor is performed on substrates mainly based on various types of hardwood sawdust, while other tree sawdust (deriving from apple or cherry trees or conifers) is also used (Stamets 2011). Supplementation of such media with sorghum and wheat bran has improved mushrooms yields considerably (Guerrero et al. 2011) and so did alternative substrates such as soybean, camelina seeds, and sunflower seed cakes (Krupodorova and Barshteyn 2015).
Trametes versicolor has a long history of use in Japanese and Chinese traditional medicine. The composition of T. versicolor mushrooms has been extensively studied, and various ingredients with medicinal properties were detected. In particular, proteoglycans, mainly polysaccharide peptides (PSP) and polysaccharide K (PSK), are considered as the most representative and were shown to possess antimicrobial, antivirus, antitumor, and immunostimulatory properties. PSK is administered to cancer patients in Japan both during and after chemotherapy (Morimoto et al. 1996). On the other hand, freeze-dried T. versicolor fruit-body powder is often prescribed in the USA by homeopathic doctors and oncologists to cancer patients; positive results from such treatment are attributed to stimulation of the immune system (Fisher and Yang 2001). In addition, studies on both animals and humans demonstrated the significant effect of T. versicolor water extracts in liver protection and at reducing the level of cholesterol in blood as well as in the treatment of diabetes mellitus (Chiu et al. 1993; Hor et al. 2011).
4.8 Grifola frondosa
Grifola frondosa (maitake or hen of the woods) is a relatively rare mushroom occurring in the temperate forests of Asia, Europe, and eastern North America. It grows mainly at the base of oak and chestnut trees, but is also found on dead wood of various other plant species. G. frondosa cultivation has spread in the last two decades mainly in Japan and SE Asia, while mushrooms are recently used as dietary supplements too. Mushroom production is mainly performed in polypropylene bottles or in sterilizable bags, and the most common substrate used consists of sawdust supplemented with bran (Fig. 12.4a). However, the BE values reported from cultivation on such media are rather low, i.e., 35% for oak sawdust supplemented with corn bran (Mizuno et al. 1986), or up to 40% for oak sawdust supplemented with rye, millet, and wheat bran (Shen and Royse 2002). In contrast, the use of other substrates such as brewery waste, coffee spent ground, and olive press cake seems to adversely affect yields and quality of the mushrooms produced (Barreto et al. 2008; Gregori et al. 2009; Montoya et al. 2012; Svagelj et al. 2007), probably due to the presence of toxic compound inhibiting mycelium growth and/or fructification. Nevertheless, increase in the demand for G. frondosa mushrooms provides sound incentives for further research in order to assess the suitability of alternative plant residues as substrates for their cultivation.
The chemical composition and the medicinal properties of G. frondosa biomass have been intensely studied in recent years, and as a result, various products were manufactured deriving from mycelium and fruit-body extracts. These were found to contain large amounts of ergothioneine (up to 1840 mg kg−1) (Dubost et al. 2006) to which antioxidant and cytoprotective capabilities are attributed (Cheah and Halliwell 2012), as well as lectins, e.g., an N-acetylgalactosamine-specific lectin which could agglutinate erythrocytes and offers cytotoxic properties against HeLa cells (Kawagishi et al. 1990). Furthermore, low molecular mass polysaccharides enhancing phagocytosis of human polymorphonuclear neutrophils and an antivirus protein efficient against HSV-1 were detected (Gu et al. 2006). In addition, G. frondosa extracts presented antimicrobial, antioxidant, immunostimulatory, and antitumor properties (Klaus et al. 2015), while they could also be used in cosmetology since they stimulate collagen biosynthetic activity for fibroblasts and show photoprotection of human dermal fibroblasts (Kim et al. 2010a).
4.9 Hericium erinaceus
Hericium erinaceus (commonly known as lion’s mane or monkey’s head due to the fruit-body shape) grows on the wood of deciduous trees and produces fleshy, white mushrooms possessing distinctive elongated spines (Fig. 12.4b). It is traditionally cultivated in Asia, mainly in China, Japan, and Malaysia, by using hardwood sawdust as substrate. However, recent studies have shown that replacing part of the (or the entire) sawdust medium with various agricultural residues, such as sunflower seed hulls (Figlas et al. 2007), sugarcane bagasse, rice hull and/or soybean dregs (Hu et al. 2008), and olive pruning (Koutrotsios et al. 2016), does not only increase productivity but also upgrades mushroom content in bioactive components like antioxidants, phenolics, and α- and β-glucans (Koutrotsios et al. 2016). In general, BE values reported from various H. erinaceus cultivation substrates ranged from 31 to 70% (Figlas et al. 2007; Ko et al. 2005; Koutrotsios et al. 2016).
A large number of bioactive substances have been isolated from H. erinaceus and were investigated for their medicinal properties in vitro and in animal and human preclinical trials. Among them, 20 aromatic compounds contain a benzene ring, i.e., hericenone A to L, erinacine A to D, and 3-hydroxyhericenones (Ma et al. 2010a, b; Ueda et al. 2008); several of the hericenones were shown to stimulate the synthesis of nerve growth factors and to have an anti-dementia effect in experimental studies on rats and humans. Furthermore, these compounds demonstrated additional medicinal properties, including cytotoxic, antibiotic, and protective against endoplasmic reticulum stress-dependent cell death (Kawagishi et al. 1994a, b; Ma et al. 2010a; Ueda et al. 2008). Other bioactive compounds detected in H. erinaceus include diterpenoids (some of which, e.g., cyathane terpenoids, erinacine A to G, promoting biosynthesis of nerve growth factors in cell cultures; Kawagishi et al. 1994a, b) and several lectins with hemagglutinating activity (Gong et al. 2004) or with an effect on adhesive properties of erythrocytes (Kawagishi et al. 1994a, b).
4.10 Volvariella volvacea
Volvariella volvacea, commonly known as paddy straw mushroom, is a saprotrophic species fruiting under high temperatures (>30 °C), whose commercial production reaches 180,000 tons per year, making it the sixth largest mushroom crop in the world (Biswas and Layak 2014). It is traditionally cultivated on non-composted and unpasteurized bundles of paddy straw or banana leaves which are laid outdoors to form beds or are placed within wooden frames (Reyes 2000). However, low mushroom yields are often obtained since substrates are rather poor in nutrients and are exposed to contaminations and irregular environmental conditions. In contrast, indoor cultivation provides the prerequisites for higher productivity, as demonstrated by several pertinent studies employing composting and pasteurization of paddy straw supplemented by molasses and NPK fertilizer (Reyes 2000), wheat straw supplemented by wheat or rice bran, and cotton waste or paddy straw (Rajapakse 2011). Moreover, the use of other agricultural by-products, e.g., dried banana leaves and sugarcane bagasse (Oei 2003), oil farm bunch waste (Thiribhuvanamala et al. 2012), and cocoa bean shells (Belewu and Lawal 2003), led to two to three times increase of BE and more stable production yields. In addition, since cellulose/lignin ratio was demonstrated to be positively correlated with V. volvacea mycelium growth and mushroom productivity (Philippoussis et al. 2001), the exploitation of additional plant residues is worth examining.
V. volvacea mushrooms contain high amounts of essential amino acids as well as vitamins, polypeptides, steroids, terpenoids, lectins, and phenolic compounds (Chang and Buswell 1996; Hung and Nhi 2012). Furthermore, the proteins volvatoxin and flammutoxin, as well as polysaccharides isolated from this fungus, are considered to possess antitumor properties (Cochran 1978). V. volvacea contains larger amounts of γ-aminobutyric acid (999–1150 mg/kg) (Table 12.2) than most other cultivated mushrooms; this compound plays a crucial role in reducing neuronal excitability throughout the nervous system and is also directly responsible for the regulation of muscle tone in the human body. In addition, various extracts from paddy straw mushrooms were found to present high antioxidant properties and could, therefore, contribute to the prevention of cardiovascular and neurodegenerative diseases (Cheung et al. 2003; Joseph et al. 1999).
5 Conclusion
The medicinal use of mushrooms has a very long tradition, especially in Asia, while pertinent interest in Western countries began to develop in the last decades only. Nowadays, research has focused on the investigation of the mechanisms of action of several bioactive compounds isolated from mushrooms and on clinical trials. In particular, those deriving from cultivated species present an enormous – yet largely untapped – potential of applications related to biotechnology, biomedicine, pharmacology, etc. Therefore, mushrooms could significantly contribute not only to the development of such economic activities but most importantly at the generation of potent medicinal products of natural origin through the valorization of lignocellulosic substrates commonly regarded as waste materials.
Abbreviations
- BL:
-
Banana leaves
- BP:
-
Bracts of pineapple crown
- BS:
-
Broadleaf sawdust
- BST:
-
Barley straw
- BWC:
-
Broadleaf wood chip
- c:
-
Composted
- CB:
-
Corn powder
- CC:
-
Corn cobs
- CH:
-
Coffee husk
- CP:
-
Coffee pulp
- CS:
-
Corn stover
- CSG:
-
Coffee spent ground
- CSH:
-
Cotton seed hulls
- CW:
-
Cotton waste
- EFB:
-
Palm empty fruit bunches
- GM:
-
Grape marc
- HH:
-
Hazelnut husks
- HR:
-
Herbs residue
- NS:
-
Nut shells
- OL:
-
Olive leaves
- P:
-
Paper
- PN:
-
Pine needles
- PPF:
-
Palm pressed fiber
- PS:
-
Paddy straw
- RS:
-
Rice straw
- SB:
-
Sugarcane bagasse
- SL:
-
Sugarcane leaves
- SSH:
-
Sunflower seed hulls
- TPOMW:
-
Two-phase olive mill waste
- VP:
-
Vineyard pruning
- WB:
-
Wheat bran
- WP:
-
Waste paper
- WPS:
-
Weed plants
- WS:
-
Wheat straw
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Zervakis, G.I., Koutrotsios, G. (2017). Solid-State Fermentation of Plant Residues and Agro-industrial Wastes for the Production of Medicinal Mushrooms. In: Agrawal, D., Tsay, HS., Shyur, LF., Wu, YC., Wang, SY. (eds) Medicinal Plants and Fungi: Recent Advances in Research and Development. Medicinal and Aromatic Plants of the World, vol 4. Springer, Singapore. https://doi.org/10.1007/978-981-10-5978-0_12
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Publisher Name: Springer, Singapore
Print ISBN: 978-981-10-5977-3
Online ISBN: 978-981-10-5978-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)