Liquid Fermentation of Edible and Medicinal Fungi

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This entry is adapted from the peer-reviewed paper 10.3390/foods12102086

Liquid fermentation of edible and medicinal fungi involves cultivating and growing fungi in a liquid medium, providing optimal conditions for their growth and fermentation. This method offers advantages over traditional solid-state fermentation, such as better control of environmental factors, higher yield and purity, and faster production cycles. It also enables the extraction of bioactive compounds with therapeutic potential, which can be utilized in pharmaceuticals, nutraceuticals, cosmetics, and functional foods. Overall, it is a modern technique for producing high-quality fungal products with enhanced bioactive properties.

edible and medicinal fungi liquid fermentation

1. Introduction

During the mycelial growth of edible and medicinal fungi, the metabolism will secrete a large amount of nutrients and active ingredients that can be extracted from both the mycelium and extracellular fluid. These nutrients and active ingredients contain many active substances such as polysaccharides, triterpenes, proteins, amino acids, vitamins, alkaloids, glycosides, sterols, flavonoids and antibiotics. Among these, triterpenes, polysaccharides and proteins are the most widely studied. They have immunoregulatory, anti-tumor, antioxidant, anti-viral, hypoglycemic and lipid-lowering properties.

2. Main Components of the Liquid Fermentation of Edible and Medicinal Fungi

2.1. Polysaccharides

The liquid fermentation of polysaccharides from edible and medicinal fungi can be divided into intracellular polysaccharides (IPSs) and extracellular polysaccharides (EPSs), or they can be divided into glucans and heteropolysaccharides according to the sugar composition. Glucans are composed of single glucose, which can be further divided into α configuration and β configuration in space conformation, and the active glucans in edible and medicinal fungi are mainly of the β configuration; heteropolysaccharides are composed of a variety of monosaccharides with different molar ratios, and the most common monosaccharide composition of mycelium from edible and medicinal fungi is fructose, xylose, mannose and ribose ^[1].

Fermented polysaccharides have anti-tumor, immunity improvement and anti-oxidative functions. Jing et al. ^[2] isolated two exopolysaccharide components with different molecular weights from Pleurotus eryngii that have antioxidant and anti-tumor effects; among them, the low molecular weight exopolysaccharides with better solubility has greater activity. Assis et al. ^[3] found that the EPSs from Pleurotus ostreatus have anti-tumor activities. Luo et al. ^[4] separated and purified the extracellular homogeneous polysaccharide EPS-2-1 and intracellular polysaccharide IPS-2-1 from liquid fermented Ganoderma lucidum, and the polysaccharides had the ability to scavenge the DPPH and hydroxyl radicals, while EPS-2-1 had better antioxidant ability. Du et al. ^[5] isolated an exopolysaccharide with a molecular weight of 2900 kDa from the mycelium extracted from the submerged culture of Schizophyllum schizophyllum. Polysaccharides can inhibit the expression of nitric oxide synthase induced by LPSs (lipopolysaccharides) in vitro and have some anti-inflammatory activities.

2.2. Triterpenoids

Triterpenes from edible and medicinal fungi are lanosterane derivatives that can be divided into C24, C27 and C30 according to the number of carbon atoms. According to the structure, they can be divided into tetracyclic and pentacyclic triterpenes. According to the different functional groups and side chains, triterpenes can be divided into Ganoderma lucidum acid, Ganoderma lucidum alcohol, Ganoderma lucidum aldehyde and Ganoderma lucidum lactone. Ganoderma lucidum acid and Ganoderma lucidum alcohol are the most abundant triterpenes; according to polarity, triterpenes can be divided into medium polar triterpenes and low polar triterpenes ^[6].

Anti-tumor and antibacterial activities of triterpenoids from mycelium are their main activities. Zhu et al. ^[7] isolated four triterpenoids from the liquid fermentation of Ganoderma lucidum mycelium through silica gel column chromatography, reversed-phase column chromatography and methanol recrystallization; the isolated triterpenoids inhibited the proliferation of tumor cells K562 and L1210. Cai et al. ^[8] investigated the antibacterial effects of total triterpenes from fermented Phellinus linteus. The results showed that the total triterpenes from Phellinus linteus had inhibitory effects on Escherichia coli Y35, Staphylococcus aureus, Bacillus subtilis and Bacillus thuringiensis; the results of anti-tumor tests showed that the extract could strongly inhibit the proliferation of colon cancer cells CaCO₂, and a flow cytometry analysis showed that it blocked the cell cycle and induced the programmed apoptosis of CaCO₂. The antioxidant activity of 300 ug/mL total triterpene extract on hydroxyl radical, superoxide anion, DPPH radical and ABTS was over 90%. Zhou et al. ^[9] discovered five triterpenes with lipoxygenase inhibition from triterpene extracts using high performance liquid chromatography–electrospray ionization mass spectrometry (HPLC-ESI-MS).

2.3. Proteins

Proteins are abundant in edible and medicinal fungi, their content is generally between 20 and 50% (dry weight), and the proportion of essential amino acids is reasonable ^[10]. Kurbanoglu et al. ^[11] studied the submerged culture of Agaricus bisporus in ram horn hydrolysate, and its protein concentration was 47%; an amino acid analysis showed that Agaricus bisporus protein contained many essential amino acids and it had high nutritional value. Rahgo ^[12] optimized the fermentation medium of a new variety of Morchella esculenta obtained in northern Iran, and the protein content reached 38% (including 28.7% essential amino acids).

There are many nutritional evaluation indexes for edible fungal proteins, such as biological evaluations, non-biological evaluations, comprehensive evaluations based on the essential amino acid composition, digestibility, etc. Gang et al. ^[13] evaluated the proteins and amino acids in liquid fermented Cordyceps militaris, and the protein content was 21.1%. The amino acid score AAS, chemical score CS, essential amino acid index EAAI, biological value BV, nutritional index NI and amino acid correlation ratio SRCAA were recorded at 62.41, 38.74, 88.37, 84.63, 18.61 and 25.57, respectively. The protein content was 2.52% higher than the model value of the total essential amino acids of eggs and was 45.57% higher than the FAO/WHO model value.

3. Comparison of the Main Components of Edible and Medicinal Fungi in Liquid Fermentation and Fruiting Body Cultivation

The main active components isolated from the fruiting bodies of edible and medicinal fungi are polysaccharides, triterpenes, proteins, alkaloids, sterols, etc. These active substances exhibit anti-tumor, immunoregulatory, antioxidant, hypoglycemic and lipid-lowering effects ^[14]^[15]. The active components that are separated during liquid fermentation are basically the same as those from fruiting bodies, and the content of some important active components, such as polysaccharides from liquid fermentation, is higher than that from the fruiting bodies. Some studies also proved that there are some components in fruiting bodies that are not found in mycelium such as some triterpenoids. Liu et al. ^[16] compared the polysaccharide, triterpene, alditol and nucleoside contents between Ganoderma lucidum fruiting body and the liquid fermented mycelium. The results showed that the polysaccharide content in mycelium was 1.54%, which was significantly higher than that in the fruiting body (0.79–0.87%); the molecular weight distribution of the mycelium polysaccharides was 2.31 × 10⁵ Da, while that of the fruiting body was 3.27 × 10⁴–1.95 × 10⁶ Da. They both contained arabinitol and mannitol, and the mycelium also contained a small amount of erythritol. The nucleoside content in mycelium was lower than that in the fruiting body, but the cytidine, guanosine and adenosine contents were higher in the fermented mycelium. Ten triterpenes were detected in the fruiting body, but only Ganoderma lucidum acid A and G. lucidum keto-triol were detected in the mycelium with greater content. Zhang ^[17] also found that the fermented mycelium and fruiting body of Ganoderma lucidum had some of the same components, but their contents were different; the crude polysaccharide and polysaccharide contents of mycelium were 2.26 times and 3.5 times higher than those in the fruiting body, and the crude protein content was 2.47 times higher than that in the fruiting body. The essential amino acids of the fruiting body accounted for 58.4% of the total amino acids, while the proportion in the mycelium was 45.2%.

Some studies have shown that there may be different results in the evaluation of proteins and amino acids in edible and medicinal fungi using different evaluation criteria for the nutritional value. Xi et al. ^[18] evaluated the protein of the lotus leaf fruiting body and mycelium, and found that the nutritional values of the fruiting body and mycelium were slightly different; For example, the amino acid composition of the proteins from the fruiting body was closer to that of standard egg white, but the amino acid composition of the proteins from the mycelium was closer to the FAO/WHO model. However, the nutritional value of the mycelium was better than that of the fruiting body considering the nutritional balance, and the proportion of essential amino acids in the fruiting body was 40.2%, which was higher than that in mycelium (35.3%). Some amino acids in mycelium, such as lysine and leucine, were higher than those in the fruiting body, while others were close to those in the fruiting body. The protein content in mycelium fermentation broth was low, only six amino acids were found including valine and tyrosine. The chemical score and amino acid score of mycelium were 73.4 and 80.2, respectively, which were significantly higher than those of the fruiting body: 45.4 and 57.8. The essential amino acid index of the fruiting body was 76.8 and that of mycelium was 70.7. The nutritional value of mycelium proteins was slightly lower than that of the fruiting body, but the nutritional index of the fruiting body was 16.4, which was lower than that of mycelium: 20.0.

Table 1 summarizes the nutritional components of the mycelium and fruiting bodies of edible and medicinal fungi observed in the literature, and the results show that there is little difference in the nutritional components between the fruiting bodies and mycelium. In some species, the total sugar, protein and other nutrients in mycelium are higher than that in the fruiting bodies. while in other species, the outcome is quite different. However, the crude fiber of mycelium from edible and medicinal fungi listed in Table 1 are all lower than that of the fruiting bodies, which may suggest that mycelium may be more beneficial for human absorption and utilization.

Table 1. Nutrient composition difference between the fruiting bodies and fermented mycelia from different edible and medicinal fungi (g/100 g dry weight).

Variety	Origin	Polysaccharide	Triterpenes	Amino Acid	Crude Protein	Protein	Fat	Fiber	Ash	Total Sugar	References
Ganoderma leucocotextum	Mycelia	1.54	0.03	-	-	-	-	-	-	-	^[16]
Ganoderma leucocotextum	Fruiting body	0.79–0.87	0.07–0.09	-	-	-	-	-	-	-	^[16]
Ganoderma sp.	M	5.43	-	25.57	-	2.16	-	-	-	-	^[17]
Ganoderma sp.	F	1.55	-	8.61	-	0.60	-	-	-	-	^[17]
Lyophyllum decastes	M	1.77	-	-	28.30	-	2.78	5.32	6.06	54.7	^[18]^[19]
Lyophyllum decastes	F	3.55	-	-	21.40	-	1.44	9.52	13.6	53.04	^[18]^[19]
Ganoderma lucidum	M	-	-	-	27.42	19.22	8.12	1.06	6.98	30.54	^[20]
Ganoderma lucidum	F	-	-	-	8.88	6.22	6.6	18.10	5.54	22.34
Ganoderma sinense	M	-	-	-	30.02	21.04	8.34	1.94	4.26	29.46
Ganoderma sinense	F	-	-	-	16.39	11.48	7.80	14.6	3.70	17.00
Ganoderma lucidum (Chuanzhi no.6)	M	-	-	-	29.95	20.99	9.77	1.22	11.44	22.60
Ganoderma lucidum (Chuanzhi no.6)	F	-	-	-	15.66	10.97	8.60	13.70	3.09	19.60
Grifola frondosa	M	-	-	-	21.70	-	2.53	10.34	6.05	57.20	^[21]
Grifola frondosa	F	-	-	-	31.50	-	1.70	10.70	6.41	49.70	^[21]
Dictyophora indusiate	M	-	-	-	24.82	-	2.09	6.60	-	51.50	^[22]
Dictyophora indusiate	F	-	-	-	17.87	-	0.63	11.47	-	54.98	^[22]
Cordyceps militaris	M	3.44	-	17.65	-	-	-	-	-	-	^[23]
Cordyceps militaris	F	2.75	-	18.71	-	-	-	-	-	-	^[23]
Volvariella bombycina	M	-	-	0.44		0.35	0.36	1.11	0.35	6.30	^[24]
Volvariella bombycina	F	-	-	12.10		22.55	1.88	11.41	11.62	58.60	^[24]
Fomitopsis pinicola	M	-	-	43.89		45.76	2.84	0.70	4.76	42.36	^[25]
Fomitopsis pinicola	F	-	-	1.53–3.81		4.71–7.06	14.50–16.80	1.04–1.09	0.50–1.42	70.83–72.97	^[25]

4. Biological Activity of the Liquid Fermented Products of Edible and Medicinal Fungi

Liquid fermented mycelium and extracellular extracts of edible and medicinal fungi have anti-tumor, immunoregulatory, antioxidant, antibacterial and antiviral activities.

4.1. Anti-Tumor

The anti-tumor effect of edible and medicinal fungi can be manifested in the prevention of tumor occurrence and the killing effect of the produced tumor. Gao ^[26] investigated the anti-tumor activity of ethanol extract from the fermented mycelium of Agaricus blazei in vivo and in vitro. The results showed that the semi-inhibitory concentration of the extract on the human hepatoma cell Bel-7402 was 1507 μg/mL, and it also had a certain effect on the inhibition of the S180 tumor in tumor-bearing mice with a life prolongation rate of 52.94%. Huang et al. ^[27] found that Ganoderma pine mycelium and fermentation broth could inhibit the proliferation of H22 liver ascites tumor cells by improving the immune function in mice. Fijakowska et al. ^[28] found that indole, phenol and sterol compounds contained in the mycelium of Laminophyllum hadcertain antioxidant and inhibitory proliferation effects on A549 lung cancer, DU145 prostate cancer and A376 melanoma cells. Yu ^[29] investigated the inhibition rate of Tricholoma matsutake crude polysaccharides on three kinds of human tumor cells. The results showed that the inhibition rates of 10 mg/mL polysaccharides on melanoma B16, liver cancer cell SMMC7721 and cervical cancer cell Hela were 63.54%, 62.43% and 57.81%, respectively. Zhu et al. ^[7] isolated four triterpenoids from the liquid fermented mycelium of Ganoderma lucidum and found that they could effectively inhibit the proliferation of K562 and L1210 tumor cells. Li ^[30] investigated the anti-tumor effect of Ganoderma lucidum polysaccharides and tetracyclic triterpene acid. The results showed that the average inhibition rate of a single polysaccharide was 51.2%, and that of mixed samples reached 68.0%. The results provide a reference for the effective compound use of fermented products.

4.2. Immunoregulation

The immunomodulatory effect of polysaccharides from edible and medicinal fungi is the basis of other functions such as anti-tumor effect. SPG, an intracellular homogeneous polysaccharide of Schizophyllum was isolated by Li ^[31], and it was determined that it could restore the proliferation response of spleen lymphocytes in aged mice and could ameliorate the delayed skin allergic reaction of mice induced by DNBC. It also increased the level of mouse splenic orifice forming cells induced by sheep red blood cells in adult mice and improved the cellular and humoral immune functions of aged mice. Li ^[32] isolated three kinds of homogeneous polysaccharides from the liquid fermented mycelium of Umbrella dinghuensis and studied their immune activity in the mouse model. The results showed that the three polysaccharides could restore the immunity induced by cyclophosphamide and at the same time improve the spleen index, ear swelling from a delayed type of hypersensitivity and lysozyme activity in spleen and serum at the same time. Carrieri et al. ^[33] extracted a water-soluble heteropolysaccharide GLP-3 from Ganoderma lucidum mycelium, and it was determined that it could be recognized by the toll-like receptor, and play an immunomodulatory role by activating MAPKS, PI3K)/Akt and NF-κ B signaling pathways in macrophage RAW264.7.

4.3. Antioxidant

The mycelium and extracellular fluid extracts of various edible and medicinal fungi have antioxidant effects. Hu ^[34] purified an irregular linear homogeneous polysaccharide PHEB with a molecular weight of 36.1 kDa from the fermented mycelium of Hericium erinaceus, which can ameliorate neuronal damage in the brain of Alzheimer’s disease mice. Li ^[32] purified three polysaccharide components from the fermented mycelium of Umbrella dinghuensis, which have antioxidant activities for scavenging hydrogen peroxide, DPPH radical and hydroxyl radical, and chelating ferrous ions (Fe²⁺). Liu ^[35] found that the scavenging activity of the exopolysaccharides of Inonotus obliquus on the DPPH and hydroxyl radicals was better than that of mycelial polysaccharides. Zhang et al. ^[36] extracted the mycelial protein of Morchella esculenta through alkali dissolution and acid precipitation, and the protein was determined to have antioxidant properties for scavenging hydrogen peroxide, DPPH radical and hydroxyl radical, and the IC50 values of the total antioxidant capacity and reducing power were 6.93 mg/mL and 4.24 mg/mL, respectively.

4.4. Antibacterial and Antiviral

Studies have shown that many kinds of edible and medicinal fungi fermentation broth sand their extracts have inhibitory effects on common bacteria. Dou et al. ^[37] investigated the antibacterial effect of liquid fermentation broth from seven common edible and medicinal fungi, such as Lentinus edodes and Coprinus comatus, on three drug-resistant fungi: Streptococcus pneumoniae, Staphylococcus aureus and Escherichia coli. The results showed that the fermentation broth of edible and medicinal fungi had good antibacterial activity against Staphylococcus aureus The diameter of the antibacterial zone of Flammulina velutipes fermentation broth was 6.733 mm, and the antibacterial rate was 58.586%. The bacteriostatic activity of the fermented broth of edible and medicinal fungi against Streptococcus pneumoniae was low, the diameter of the bacteriostatic zone of Coprinus comatus fermented broth was 4.433 mm, and the bacteriostatic rate was 30.370%. The inhibition rate of the tested edible and medicinal fermentation broth against Escherichia coli was less than 10% which showed that the inhibition effect is not good.

5. Comparison of the Active Substances in Liquid Fermented Mycelium and the Cultivated Fruiting Body of Edible and Medicinal Fungi

The difference in nutritional composition or proportion between the fruiting body and mycelium of edible and medicinal fungi leads to different efficacies or different levels of efficacy, and this provides a basis for enterprises to select suitable products for application. Due to the different types of products, such as the different varieties, different cultivation or fermentation conditions, the existing studies on the efficacy of fermentation products and cultivation products of the same variety are limited. Yu et al. ^[38] proved that Ganoderma lucidum (G0109) mycelial polysaccharides could stimulate more NO production by macrophage Raw264.7 than the fruiting body polysaccharides, especially at low doses, and this may be related to the differences in the polysaccharide content, molecular weight, monosaccharide composition and configuration. Cai et al. ^[39] investigated the antioxidant activity of Ganoderma lucidum fruiting body and mycelium, and found that the water extract of the fruiting body had the strongest scavenging ability for the hydroxyl radical, and the water extract of mycelium had the strongest scavenging ability for hydrogen peroxide. Zhang et al. ^[40] investigated the differences in composition and activity between the fermented mycelium and the fruiting body of Phellinus linteus in four extraction phases: petroleum ether, chloroform, ethyl acetate and n-butanol. The results showed that the content of total flavonoids in the ethanol extract of mycelium was higher than that in the fruiting body, and the antioxidant activity from each phase of mycelium was higher than that of the fruiting body, while the anti-tumor activity of the fruiting body was higher than that of mycelium, suggesting that there was a significant correlation between the antioxidant activity and total flavonoids content. Chen et al. ^[41] optimized the alkali extraction and acid precipitation extraction method of Pleurotus ostreatus mycelium protein. Under the best extraction conditions, the extraction rate of mycelium protein reached 39.02%, and its emulsifying property was 48%, which was higher than that of the fruiting body protein (6%), but the foaming property of the fruiting body protein was relatively better. This conclusion also provided reference for the differential application of Pleurotus ostreatus mycelium protein and the fruiting body protein.

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Subjects: Microbiology

Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :

Meng-Qiu Yan

Jie Feng

Yan-Fang Liu

Dian-Ming Hu

Jing-Song Zhang

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Update Date: 21 Sep 2023

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