Green Biotechnology of Oyster Mushroom (Pleurotus ostreatus L.): Comparison
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The field of biotechnology presents us with a great chance to use many organisms, such as mushrooms, to find suitable solutions for issues that include the accumulation of agro-wastes in the environment. The green biotechnology of mushrooms (Pleurotus ostreatus L.) includes the myco-remediation of polluted soil and water as well as bio-fermentation. The circular economy approach could be effectively achieved by using oyster mushrooms (Pleurotus ostreatus L.), of which the substrate of their cultivation is considered as a vital source for producing biofertilizers, animal feeds, bioenergy, and bio-remediators. Spent mushroom substrate is also considered a crucial source for many applications, including the production of enzymes (e.g., manganese peroxidase, laccase, and lignin peroxidase) and bioethanol. The sustainable management of agro-industrial wastes (e.g., plant-based foods, animal-based foods, and non-food industries) could reduce, reuse and recycle using oyster mushrooms. 

  • agro-industrial residues
  • waste recycling
  • pollutants
  • bio-fermenter
  • myco-remediator
  • white-rot fungi

1. Introduction

Green biotechnology is the use of scientific techniques and tools, including molecular markers, genetic engineering, molecular diagnostics and tissue culture, on plants; it is called red biotechnology in the medical field and white biotechnology in the industrial field [1]. Fungi have several applications in agricultural and environmental sustainability, which can support the growth of plants, such as mycorrhizal association [2], for human nutrition, including edible mushrooms [3][4]. Arbuscular mycorrhizal fungi can also be utilized to sustain and improve soil health [5]. Fungi, such as mushrooms, are important plants, which can be consumed due to their nutritional benefits (as edible mushrooms) and their medicinal values (as medicinal mushrooms) since time immemorial [6]. Many applications of mushrooms were confirmed by researchers, such as their valuable biotechnological properties [7][8], the sustainability of the mushroom industry through a zero waste and circular bioeconomy [9], and myco-remediation [10].
The genus Pleurotus is considered as the second most cultivated and distributed edible mushroom all over the world after the champignon mushroom (Agaricus bisporus), because of its adaptation capability [11][12][13]. The mushrooms of Pleurotus are characterized by several valuable medical, biotechnological, and nutritional attributes. Numerous studies have reported the many relevant features of the Pleurotus genus, which confirmed their attractive low-cost industrial tools that resolve the pressure of ecological issues [7][11][12][14][15][16][17]. These issues may include the production of enzymes (oxidases and hydrolases) and biomass from fruit residues using Pleurotus spp. [18], bioethanol production [19], the biodegradation of pollutants [20][21], and medicinal attributes [6]. This genus is also characterized by its high content of fatty acids, steroids, and polysaccharides, which can produce a lot of bioactive molecules and has become a popular functional food [15]. Additionally, a number of Pleurotus species are highly adaptive, possess specific resistance to pests and polluted diseases, and they do not require any specific conditions for their growth [7]. P. ostreatus is an important member of the Pleurotus species, which has significant medicinal importance and nutritional values [22] due to its anti-oxidative, anti-carcinogenic, anti-inflammatory, anti-hypercholesteremic, anti-viral, and immune-stimulating properties [11].

2. The Genus Pleurotus and Its Potential Uses

2.1. Taxonomy and Botanical Description

The Pleurotus species belongs to the Kingdom of Fungi, Phylum of Basidiomycota, Class of Agaricomycetes, Order of Agaricales, Family of Pleurotaceae, and the Genus of Pleurotus [23] (Figure 1). Pleurotus species, such as many species of mushrooms, include cultivated and wild mushrooms, which are dominant in many forests worldwide. Pleurotus was first scientifically described in 1775 and, in 1871, the German mycologist Paul Kummer transferred the oyster mushroom to the genus Pleurotus. This is a new genus defined by Kummer himself in 1871 and is the currently accepted scientific name. Pleurotus ostreatus grows throughout the United Kingdom, Ireland, and most parts of Europe. It is also widely distributed in many parts of Asia, including Japan, and is located in parts of North America [24].
Figure 1.
 Photos of 
Pleurotus ostreatus
 and the scientific classification of this mushroom. (Photos were taken by Gréta Törős, Debrecen University, Hungary).

2.2. Food Importance of the Pleurotus Genus

The genus Pleurotus includes more than 200 species, which are consumed worldwide as edible mushrooms with an annual increase of 15%, and Pleurotus is considered as the second most commonly consumed mushrooms [25]. Some representatives of this genus (e.g., the oyster mushroom or P. ostreatus) are well known for their odor, flavor, nutraceutical value, and gastronomic properties, which are important to several consumers [26]. Thus, the edible mushroom of P. ostreatus has been used as a source of food additives due to its high content of antioxidants, bioactives, and β-glucans [25][27]. Due to their contents of minerals, fibers, lipids, and vitamins, Pleurotus mushrooms have become increasingly appealing as functional foods [16]. Different species of Pleurotus mushrooms and the chemical composition of their nutritional values, including moisture, proteins, carbohydrates, fats, ash and fiber, are presented in Table 1. Based on this Table, the highest content of crude proteins (30 and 35.5%, respectively) was recorded for the Pleurotus citrinopileatus and P. djamor var. roseus mushrooms, whereas the P. eryngii mushroom had the highest fiber content (28.29%).
Table 1. The nutritional content (as % or g/100 g of dried mushrooms) of some Pleurotus spp. mushrooms from different sources.
Pleurotus spp. Moisture (%) Proteins (%) Carbohydrates (%) Fats (%) Ash (%) Fiber (%) Refs.
Pleurotus ostreatus 90.7 18.3 71.25 2.58 7.82 14.31 [28]
Pleurotus eryngii 91.0 11.9 39.85 7.50 4.89 28.29 [29]
Pleurotus eryngii 88 20 53 2.8 7.5 7.5 [30]
Pleurotus eryngii 88 18.8 57 2.3 5.5 10 [31]
P. citrinopileatus 88.9 30.0 42.50 3.90 7.65 20.78 [32]
Vitamin E Lipid peroxidation is prevented in cell membranes [43] Pleurotus flabellatus 91.0 21.6 57.40 1.80 10.7
Immuno-modulatory Polysaccharides The toxicity of cyclophosphamide in mice was decreased due to the immune-modulatory activity [4311.90 ][33]
P. djamor var. roseus 79.5 35.5 44.75 1.72 5.90 14.60 [34]
Anti-inflammatory Polysaccharides (β-glucans) Methotrexate may have a synergistic effect on the arthritis of rats [45] Pleurotus pulmonarius 78.8 20.3 34.00 2.62 7.33 9.00 [
Anti-hypercholesterolemic Statins (lovastatin) In the cholesterol synthesis pathway, 3-hydroxy-3-methyl-glutaryl coenzyme A reductase is inhibited due to the conversion of enzymes to mevalonic acid35]
[46] Pleurotus djamor 86.8 24.1 45.59 4.73 9.84 15.91 [36]
  Flavons (chrysin) Non-enzymatic antioxidant parameters in hypercholesterolemic rats, the blood/serum levels of lipid profile parameters and hepatic marker enzymes decreased [47] Pleurotus tuber-regium 87.1 22.1 63.03 1.06 2.97 10.86 [37]
Anti-cancer and anti-tumor Pleurotus florida 87.5 20.5 42.83 2.31 9.02 11.50 [38]
Pleurotus sajor-caju 87.0 24.6 39.82 2.29 8.28 10.90 [39]
Pleurotus cystidiosus 91.1 15.6 55.92 2.05 6.30 20.05 [22]
In 2017, the world production of P. ostreatus was approximately 4.1 million tons. Similar to many oyster mushrooms, P. ostreatus is cultivated for foods and medicinal purposes. It can be cultivated on different lignocellulosic substrates, including maize cobs, wheat straw, sawdust, or cotton waste [40]. Pleurotus spp. can colonize and bio-degrade a large variety of lignocellulosic wastes, as a result of their ability to produce many ligninolytic enzymes [40]. Pleurotus mushrooms have been used for their high nutritive content and their potential biotechnological and environmental applications.

2.3. Medicinal Importance of the Pleurotus Genus

This genus includes more than 40 species, commonly referred to as the “Oyster mushroom”, including P. ostreatus and P. eryngii, which has attracted special attention because of its high nutritional values and medicinal attributes [11][12]. It is well known for its anti-oxidative, anti-carcinogenic, anti-inflammatory, anti-viral, anti-hypercholesteremic, and immune-stimulating properties, as well as its ability to regulate glucose levels and blood lipids [11][12]. Table 2 lists the bioactive compounds and their activities, which are dominant in Pleurotus ostreatus and their mode of actions or mechanisms [41].
Table 2. Different bioactive compounds of Pleurotus ostreatus and their mode of actions.
Activity Bioactive Compound Mode of Action Refs.
Anti-oxidative Lectins The dendritic cells were activated using the pathway of “Toll-like receptor 6 signal” [42]
  Polysaccharides Increasing the activities of SOD, CAT, GST, GR, APx and reducing superoxide radicals, and the activity of GPx [43]
  Phenols Inhibits the growth of HL-60 cells by inducing apoptosis [44]
  Flavonoids, ascorbic acid and β-carotene Induces apoptosis by inhibiting HL-60 cell growth [44]
 
Polysaccharides
In HeLa cell lines, cytotoxic activity inhibited the development of Ehrlich Tumor and Sarcoma 180 (S-180)
[45][48]
  Pleuran (β-glucan) Anti-neoplastic properties of different cells (breast, colorectal and prostate cancers) [48]
  Proteins In cell line SW 480, therapeutic effects on colorectal cancer and monocytic leukemia by inducing apoptosis [48]
  Lectins Tumor burden in Sarcoma S180 reduced by 88.4% and hepatoma H-22 by 75.4% in mice; increase in survival time [45]
Anti-viral and anti-microbial Laccase Anti-viral effects against hepatitis C [48]
  Ubiquitin-like protein Anti-viral effects in human immunodeficiency viruses, such as HIV-1 [45]
  Nanoparticles mixed with aqueous extract Inhibiting the growth of Gram-negative bacteria [45]
  Ribonucleases Degradation of viral genetic materials to neutralize HIV [49]
Hepatoprotective Poly-saccharopeptides Thioacetamide is alleviated, inducing alterations in inflammation, steatosis, fibrosis and necrosis [49]
Anti-aging Mushroom powder Significant bifidogenic and then strong lactogenic effects [50]
Abbreviations: HIV-1 (human immunodeficiency viruses), SOD (superoxide dismutase), CAT (catalase), APX (ascorbate peroxidase), GR (glutathione reductase), GST (glutathione S-transferases).

3. General Features of Pleurotus ostreatus

Pleurotus ostreatus is found in dead and living tree branches, especially hornbeam (Carpinus sp.), beech (Fagus sp.), willow (Salix sp.), poplar (Populus sp.), birch (Betula sp.) and the common walnut (Juglans regia) trees [51]. This species produces grouped fruiting bodies of various sizes, similar to oyster mushroom colonies. The fruiting body is pink, gray-to-dark brown, and is 4 to 15 cm in size. In the wild, its offspring generally appear between October and November (Figure 2). However, they can be encountered in mild winters or in early, warm springs. Their cap is 3–15 cm in diameter; broadly convex, flat or depressed flat; kidney shaped-to-fan shaped in outline, or nearly spherical when growing on tree trunks; young and fresh and somewhat greasy; bald; pale-to-dark brown; fade to buff; sometimes slowly fading and becoming two-toned; and the edge is slightly curled when young [52]. Gills can run down the trunk (or pseudo stem); close, short gills are common; and can be whitish or grayish, turning yellowish with age and sometimes with brownish edges [52]. A salient feature of these gilled mushrooms is their ability to capture and feed nematodes to the gills using a “lasso” made of hyphae. Their stem is whitish, hairy to velvety, and hard. Moreover, their flesh is thick, white and unchanging when cut.
Sustainability 14 03667 g002 550
Figure 2. The cultivation of oyster (Pleurotus ostreatus) mushrooms, the mushroom-fruiting basic processes, and how to produce a Pleurotus inoculant on a millet substrate are presented in photos 1 to 6. The mushroom fungi (Pleurotus ostreatus) culture should first be ready on the surface of the agar plate (photo 1); the cultivation substrates of oyster mushrooms are ready (photo 2); tools for the propagation of the mushroom and poured media (heat treated at 95 °C for 1 day); inoculant should be prepared, and a jar with boiled millet and oyster culture (photo 3); the millet spawn in the jar and culture media (photos 4 and 5); and finally researchers obtain the oyster mushroom. (These steps were photographed in the factory of “Magyar Gomba Kertész Kft.”, whereas all photos were taken by Gréta Törős, Debrecen University, Hungary).
These mushrooms are edible, in addition to having several important applications in biotechnological [7], nutraceutical [15][22][53], medicinal [54][55][56][57], and environmental fields [12][58]. Due to their exceptional ligninolytic attributes, the Pleurotus genus is considered as one of the most extensively investigated types of white-rot fungi. These species also have a significant role in the global initiative towards the “zero waste economy”, as a result of their ability to convert or biodegrade waste for biomass production using various enzyme properties, such as endoglucanase and laccase [12]. This distinguished role of Pleurotus spp. in the biodegradation of agro-industrial residues has been confirmed by many published reports, such as those published by Kumla et al. [59], Mahari et al. [60], Durán-Aranguren et al. [18], Ogidi et al. [61], Caldas et al. [15], and Melanouri et al. [11][12][30][31][62].
In the Pleurotus mushroom cultivation industry, it is important to meet the increased demands of human consumption of Pleurotus mushrooms, for which new methods of mushroom cultivation are needed to reduce global waste and increase mushroom productivity [34][60]. The cultivation of Pleurotus mushrooms depends on both intrinsic factors (i.e., substrate type, pH, C:N ratio, levels of spawning, surfactants, the content of N, C and moisture) and extrinsic factors, which include temperature, relative humidity, luminosity, air composition, and light [30][31][36][58][60][62][63]. The growth and cultivation of mushrooms can be achieved using growth media or substrates, which have a vital impact on the functional, chemical, and sensorial characteristics of mushrooms [58][64][65]. Solid substrates can be used traditionally in cultivating many species of mushrooms for fruiting body formation, which usually needs several months with a non-stable quality of harvested materials [66]. The technology of solid phase cultivation in the bioreactors of mushrooms can reduce the required time for producing the biomass, depending on the control of several physical process parameters, such as the aeration temperature and pH [66]. This technology may include the production of mushrooms in submerged liquid culture or sterilized solid substrates inside static or mixed chambers with a reduced amount of water, compared to submerged liquid cultivations, which allows for a nature-like growth of mycelium on the substrate [66].

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