Wild and cultivated mushrooms as food, pharmaceutical and industrial products

Wild mushrooms as industrial products. Industrial cultivated edible mushrooms are very popular as food products (Rangel- Vargas et al., 2021) widely used for preparation of medicinal drugs (Valverde et al., 2015), and constantly increasing all over the world. Thus, world production of mushrooms has increased more than 30-fold since 1978 (Royse et al., 2017). Total production of mushrooms and truffles worldwide from 2012 to 2021 augmented from 31.78 to 44.21 million metric tons (Statista, 2023); China is a leading country producing about 75% of the word's mushrooms and is the world's largest producer of Flammulina velutipes (Royse et al., 2017). The most cultivated edible mushroom genera are Lentinula which covers about 22% of the world's production followed by Pleurotus, 19% of the world's output; Auricularia, 18%; Agaricus, 15%; Flammulina, 11%; Volvariella, 5%; and others, 10% (Royse et al., 2017) (Figure 5).

Figure 5. Cultivated mushrooms in percentage of total world's production (Adapted from Royse et al., 2017).

Pleurotus ostreatus (oyster mushroom), Agaricus campestris, and Agaricus bisporus (button mushroom) are cultivated all over the world, while Lentinula edodes (former Lentinus edodes) (shiitake), Auricularia auricula (wood-ear or tree ear), Volvariella volvacea (edible straw mushroom), Flammulina velutipes (winter mushroom) and Ganoderma lucidum (red reishi) are cultivated mainly in Asia (Stabnikova et al., 2008). Nowadays the mushroom production on a large scale is going in a form of so called solid state fermentation. However, there are two traditional methods, which are still used to harvest mushrooms: (a) cultivation on wood logs and (b) on compost.

Traditional methods used for mushroom cultivation. According to Japanese and Chinese traditions, Lentinula edodes (shiitake) was grown on shii (Castanopsis cuspidata) logs until the mid-1980s. Growth of shiitake on trees requires from one to two years before the first crop of fruiting bodies could be harvested. It is possible to expedite the growth of shiitake by growing the mushrooms aseptically in plastic bags or in trays on sterilized substrate containing saw dust, bagasse, straw, paper chips and supplemented with nutrients such as starch, yeast, sugars and protein (Figure 6a). Application of this method allows their harvesting in three-four months after inoculation; the residual compost could be used as a soil fertilizer (Stabnikova et al., 2008).

The composition of medium for shiitake cultivation could be different, but the basis of the substrate should be hardwood chips and sawdust and/or cereal straw. To increase the nutritional value, medium is supplemented with bran or grain, straw of cereals, waste from the food industry and agriculture. 2-3 mm is an optimal particle size of sawdust and shavings of hardwood trees, and cereal straw is crushed to a size of 1-2 cm. Chalk or gypsum is added to improve the physical properties of the substrate. Cultivation is carried out in special chambers with the maintenance of desirable microclimate under sterile conditions or in conditions of a high degree of purity. Under the cited conditions, a yield of fruiting bodies from 15 to 30-50% from the weight of used substrate may be obtained.

Pleurotus (oyster mushroom) are much easily cultivated and the corresponding costs are lower compared to others mushroom species because these mushrooms have a shortest time to produce fruit bodies; additionally they can be grown using various lignocellulosic agricultural wastes due to their ability to produce enzyme laccase, which plays a key role in lignin degradation (Li et al., 2022). Using different waste products as substrate for cultivation of oyster mushroom species (Pleurotus ostreatus, P. cystidiosus, P. pulmonarius) allows to reduce their price to a reasonable level. It was reported that oyster mushrooms can be grown on sawdust, wood chips, cereal straw, banana leaves, peanut hull, corn leaves, wheat and rice straw, mango fruits and seeds, sugarcane leaves, hazelnut branches and husk, rice husk, spent coffee grounds, coffee pulp, grass, weed plants, olive cake, tomato tuff, pine needles, and cotton wastes (Akcay et al., 2023; Das et al., 2007; Hernandez et al., 2003; Jatwa et al., 2016; Li et al., 2022; Raman et al., 2020). For instance, lignocellulosic biomass mixture from grounded leaves of date palms (Phoenix dactylifera), wheat straw, saw dust, and boobialla (Myoporum serratum) supplemented with wheat bran and corn meal at 5% of the substrate dry weight and gypsum, 5% (Alananbeh et al., 2014). Oyster cultivation is conducted in plastic bags (Figure 6b) or trays.

Different species of Pleurotus can grow under different temperature conditions using pasteurized composed substrate or sterile non-composted one, meanwhile their fruiting bodies are relatively rarely exposed to diseases or pests. However, Pleurotus fruit bodies have short life that makes them less competitive than Agaricus bisporus and Lentinula edodes (shiitake) (Raman et al., 2020).

Figure 6. Shiitake (A) and oysters (B) cultivation in plastic bags

After harvesting of oyster mushroom fruiting bodies, “spent compost” could be used as soil conditioner to enhance soil structure; biofertilizer; animal feed due to enrichment composting material with protein by mushroom mycelium, or to use in bioremediation of soil polluted with toxic organic substances (Moore et al., 2020; Sadiq et al., 2019). Because Pleurotus has the ability for easy accumulation of heavy metals, only waste free from this contaminant could be used in mushroom production.

Auricularia auricular has different common names such as black fungus due to its dark brown to black color and wood ear or ear mushroom because of its shape. In nature this mushroom grows mainly on deciduous older trees or dead and decaying branches. It is currently the third most produced mushroom in the world and is widely cultivated in Asian countries for food and medicinal applications. China is a major producer of A. auricular, which accounts for more than 90% of the total global production and amounted 7 018 million tons in 2019 (Hao et al., 2022; Zhao et al., 2019).

This fungus possesses cellulases, xylanase, laccase and polyphenol oxidase enzymatic activity, so it is able to decompose lignin and cellulose and can be grown on lignin containing agricultural wastes. So, methods of its cultivation using compost to produce fruit bodies for food is similar to Pleurotus ostreatus. Major advantage is that cultivation of A. auricular could be done using submerged fermentation on simple liquid media for further isolation of medicinal valuable substances (Sun et al., 2016).

Cultivation of wild mushrooms in Europe was started in the 1600s when growers in Paris grew species known as Agaricus bisporus in fields, but the European mushroom industry started in the limestone caves beneath Paris at the end of the nineteenth century. This underground mushroom cultivation method has been used until our days.

Cultivation of mushrooms includes two major steps: preparation of the compost or solid medium and mycelium growth until fructification. For production of compost or medium for mushrooms cultivation, different organic and lignocellulosic materials can be used, such as wood chips, sawdust, hay, maize waste, paddy straw, cassava bagasse, waste paper, cotton seed hulls, water hyacinth, apple pomace, grape pomace oil palm bunch, husk rice, banana leaves cheese whey, horse manure, chicken manure, and others (Ivanov et al., 2021; Moore et al., 2020; Stabnikova et al., 2008).

Button mushrooms A. bisporus is one of the most cultivated species in the world, and it is the dominant fungus cultivated in Europe. In the USA, about 98% of the mushroom production comes from button mushrooms. The fruit bodies of white button of this mushroom are produced in large amounts for human consumption on a medium consisting of wheat straw, straw-bedded horse manure, chicken manure and gypsum (Straatsma et al., 2000). The materials are mixed, the ingredients are wetted, and composted for 8-9 days while temperatures will rise to 80°C during the period of uncontrolled self-heating. Then compost is packed in boxes and pasteurized for 8 h at 56-60°C and continues at 45°C for up to 7 days to remove volatile NH3 and to produce pathogen free substrate. After inoculation, compost is covered with a mixture of soil, peat, and chalk. The optimal temperature for mycelium growth is 24°C, and the optimal temperature for fruiting body production is from 14 to 18°C. The yield of mushrooms consists of around 1 kg from 1 kg of compost dry matter. Composition of compost could be changed depending on local availability of casing materials (Baysal et al., 2007).

Volvariella volvacea (paddy straw mushroom) also known as Chinese mushroom is also one of the most cultivated mushrooms of the world. It is grown mainly on rice straw, although other agricultural waste could be used. Generally, it prefers substrates with high content of cellulose and low content of lignin. Among the plant materials used for V. volvacea cultivation there are water hyacinth, oil palm bunch and pericarp waste, banana leaves, saw dust, cotton waste, and sugarcane bagasse (Ahlawat & Bindvi, 2016). Paddy straw is tied into bundles and immersed in water for 24 - 48 h. After removing excess water the straw is piled into heaps which are inoculated with V. volvacea pure cultures or spent compost from previous mushroom cultivation. The first crop of egg-like sporophores could be harvested in less than 1 month. The main disadvantage of V. volvacea production is very short shelf life even in cold storage because of autolysis. These mushrooms could be stored just for 3 days at 10 - 15oC. Therefore, straw mushrooms are best used in canned, pickled or dried form.

Ganoderma lucidum, a wood-destroying mushroom, having different pharmaceutical properties, is grown primarily for medicinal use, not as food. The common method for its cultivation is provided on wood logs or sawdust or wheat straw added with wheat bran, tea leaves and cotton husk in plastic bags or bottles. For cultivation on sawdust, addition of sucrose, 1%, and calcium carbonate, 1%, is recommended. For cultivation on wood, short pieces of wooden logs (15 cm or less in diameter and 15-24 cm in length) with moisture content of 35-40% are inoculated with mushroom mycelium, covered with soil, and then with chopped straw to ensure needed moisture and temperature. Short-log cultivation takes 4-5 months for mycelial incubation and fruiting bodies are harvested approximately after 25 days from primordia formation (Boh et al., 2007). Modern biotechnology gives the opportunity to produce mycelium biomass by their submerged cultivation in bioreactors. Cultivation of G. lucidum in synthetic liquid media is proposed for production of different valuable substances for medical use (Abdullah et al., 2020; Supramani et al., 2023; Zhao et al., 2011).

Flammulina velutipes, commonly known as golden needle mushroom or winter mushroom, is wood decaying mushroom growing in nature on the stumps of the Chinese hackberry tree, called enoki in Japanese, but also on some other trees such as aspens, willows, elms, mulberry and persimmon. Wild species have a brown color and short stem, while artificially grown ones are white with long thin stems. F. velutipes is the fifth largest edible mushroom in global production, which is especially popular in Asian countries, China, Japan, Republic of Korea, and Taiwan. F. velutipes could be cultivated on wood logs or on sawdust added with rice or wheat bran in polypropylene bags or plastic bottles (Harith et al., 2014; Sengar et al., 2019).

Solid-state and submerged liquid cultivation of mushrooms. Nowadays, for mushroom cultivation in industrial scale solid-state and submerged liquid fermentations could be used. Solid-state fermentation (SSF) involves the growth of mushrooms on a solid substrate, mainly an agro-industrial waste, meanwhile submerged cultivation is the growth of mushrooms in a liquid medium with dissolved nutrients under agitation and air supply. Application of solid substrate with low moisture content is advisable to produce mushroom fruit bodies for food or medicine, meanwhile cultivation of mushrooms in liquid media in bioreactors is a promising way to obtain mycelial biomass as an animal feed or for the production of metabolites (Letti et al., 2018).

SSF has such advantages as possibility of using a wide range of agro-industrial wastes as substrates for mushroom cultivation, relatively low energy consumption because of a lack of mechanical agitation/mixing and aeration, use of a residual substrate for bioremediation, animal feed, biofuel production, and biosynthesis of mushroom metabolites. However, when fermentation is carried out on a large scale, it is not so difficult but expensive to control the parameters of the cultivation process, such as pH, moisture content, homogeneity of substrate, concentration of oxygen, heat and mass transfer, and in addition, there is the possibility of contamination. On the other hand, SSF could be successfully used for production of certain biological active substances, for example, lignocellulolytic enzymes (Wang et al., 2019). Thus, the efficiency of SSF for the production of enzymes such as laccases, among others, is evident due to their wide industrial and technological applications; these SSF enzymatic potentialities may catalyze the oxidation of various phenolic compounds and a number of aromatic amines during the production of edible mushrooms of the genera Pleurotus (Han et al., 2020) or Ganoderma (Postemsky et al., 2017; Sharma et al., 2019).

Meanwhile, submerged cultivation is a very effective way to produce mushrooms in the form of mycelium biomass, especially for manufacturing of different valuable substances with health benefits. Liquid cultivation of mushrooms gives opportunity to control the fermentation process and final product quality and avoid contamination. The process takes place under a sterile environment in liquid medium at conditions optimal for the growth of selected mushrooms such as temperature, pH, mixing, and level of aeration (Bakratsas et al., 2021). Among the advantages of using submerged fermentation is the possibility of obtaining mushroom biomass or high-value bioactive substances in a short cultivation time for large- scale industrial applications. There are research studies devoted to production of truffles biomass using submerged fermentation, which is a promising way for business of this fungus (Tang et al., 2015). Application of liquid fermentation was proposed to produce bioactive metabolites such as triterpenoids, polysaccharides, antrodin, from medicinal mushroom Antrodia cinnamomea (Zhang et al., 2019). Cultivation of Auricularia auricular by this type of was proposed for melanin production (Sun et al., 2016). To synthesize exopolysaccharides by mycelial culture of Inonotus obliquus has also been done in liquid agitated conditions (Xiang et al., 2012).

Submerged mushroom cultivation is possible to use for production of mycoproteins, which possess high nutritional value and can be used in manufacturing of functional foods, for example in meat analogues production. Thus, cultivation of edible mushroom Pleurotus ostreatus LGAM was conducted in a stirred-tank bioreactor using aspen wood chips hydrolysate. The specific growth rate of mushroom was 1.8±0.4 d-1, biomass concentration was 25.0±3.4 g/l, and protein yield consisted of 54.5 g per 100 g of sugars (Bakratsas et al., 2023).

Unusual method for mushroom cultivation. An interesting and unusual method is used to grow edible mushrooms of Ustilago maydis (huitlacoche or cuitlacoche) in Mexico and in some areas of Central America, where it has been traditionally produced, and of the USA, where huitlacoche has been recently used, as human food. There are clear evidences in different regions of Mexico that this fungus was in the common diet of the pre-Hispanic population. The maize, Zea mays, smut termed huitlacoche is characterized by the formation of galls or tumors in maize ears (Figure 7).

Figure 7. Ustilago maydis is responsible for corn smut:

A, maize plant; B, maize cob; c, maize infected by U. maydis; D, formation of galls of tumors

Ear galls are considered an edible delicacy produced by the natural infection of the maize ears with the fungus Ustilago maydis. These smut galls are also called as maize mushrooms, Mexican truffles, or maizteca mushrooms and serve as an important food source in this country. Nowadays huitlacoche is a culinary delight for international chefs in selected places in the USA, France, Spain, Japan and others. In addition to its unique flavor, huitlacoche has been identified as a high- quality functional food and could be included into the daily diet for its attractive characteristics, selected nutrients, valuable compounds, and nutraceutical potential.

Valdez-Morales et al (2010) found that chemical composition of huitlacoche may change due to maize genotype, stage of development, plant environment, and cooking process. This composition includes, in g/100 g DM: protein, 11.5-16.4; fat, 1.6-2.3; ash, 5.2¬7.0; fiber, 16.0-23.5, and carbohydrates, 55.1-66.5 (Valverde et al., 1995). Amino acid lysine is present in huitlacoche in high amounts, 6.3 to 7.3 g/100 g protein; thus, it is an important source of this essential aminoacid, especially for consumers where cereal is the main component of the daily diet. Huitlacoche contains also high levels of polyunsaturated fatty acids with balanced ю-6/ю-3 ratio. The main fatty acid is the polyunsaturated omega-6 linoleic acid (18:2<n-6), 38.7-48.4 % from total amount of fatty acids, followed by another polyunsaturated omega-3 linolenic acid (18:3<n-3), 25.2-34.1%; saturated palmitic acid (16:0), 13.0-14.6%, and other residual fatty acids, 11.8-14.4% (Valverde and Paredes-Lopez, 1993; Valverde et al., 1995). Optimal ю-6/ю-3 ratio in foods should be less than 4:1 (Stabnikova and Paredes-Lopez, 2023); interestingly this ratio in huitlacoche varies from 1.1 to 1.9. Content of monosaccharides in huitlacoche, in mg/g of dry weight, is as follows: glucose, 140-180; fructose, 60-100; mannitol, 3.2; sorbitol, 4.5 (Juarez-Montiel et al., 2011; Valdez-Morales et al., 2010). Huitlacoche contains high amounts of phosphorus, 342.07 mg/kg, and magnesium, 262.69 mg/kg, as well as total phenolic compounds, 113.11 mg GAE/kg, and flavonoids, 28.51 mg CE/kg (Aydogdu & Golukgu, 2017). It was reported that huitlacoche possesses important functional properties, namely, antioxidant, hypocholesterolemia, immunomodulatory, anticancer, anti-inflammatory, antidiabetic and antihypertensive (Juarez-Montiel et al., 2011; Lopez-Martmez et al., 2022). Huitlacoche is sold in Mexico in domestic markets all over the country; and the commercial importance of this product is now increasing in high-income places of the U.S. and in some few other countries.

Conclusions

The role that the mushroom kingdom plays in human life is remarkable, and at the same time very important to be assessed. Simultaneously with the development of humanity, the function of mushrooms in human life has intensified and expanded. It started in the initial historical times, before the beginning of agriculture, as an additional source of nutrition, to become in the last decades as the object of large-scale industrial production using modern biotechnological procedures. The participation of mushrooms in human consumption and treatment has evolved from their use by healers and shamans to serious and careful clinical trials.

Wild edible mushrooms have a high nutritional value containing high-quality proteins, fibers, essential fatty acids, vitamins including D2, trace minerals, and such valuable compounds as polyphenols, terpenoids, sterols, while having low energetic value that allows them to be used in low-calorie diets.

Wild edible mushrooms contain many bioactive nutraceutical compounds and possess different specific pharmaceutical properties, which can be used in treatment of various serious diseases. However, more clinical trials on humans showing positive effect of orally administered mushroom consumption on health state are needed as well as regulations for food supplements with mushrooms, standards and protocols for the production and testing of mushroom products in general.

The gathering and use of wild edible mushrooms for food make a significant contribution to both the solution of the global food shortage crisis and economics of different countries around the world, and could be considered in some countries as new sources of income for local people.

The increase of interest on fungus consumption along human history at worldwide level has led to the development of basic and sophisticated techniques for their cultivation. Solid- state and submerged liquid fermentations are nowadays useful methods for cultivation of mushroom in a large-scale for their production including volumes of biomass and of very valuable specific bioactive metabolites. In brief, nowadays wild and cultivated procedures for the small and large scale production of mushrooms, and of fungal metabolites are playing, and much more will do it in the near future, outstanding roles in the use of raw materials and in the economy of populations of local people around the world; food, and pharmaceutical products and including industrial uses are their fields of utmost influence.

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