Health Promoting Benefits of Edible Mushrooms

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1		Baojun Xu	--	2312	2023-10-06 11:09:42	\|
2	format change	Peter Tang	+ 1 word(s)	2313	2023-10-07 05:17:11	\|

This entry is adapted from the peer-reviewed paper 10.3390/ijms18091934

Mushrooms have long been used for medicinal and food purposes for over a thousand years, but a complete elucidation of the health-promoting properties of mushrooms through regulating gut microbiota has not yet been fully exploited. Mushrooms comprise a vast, and yet largely untapped, source of powerful new pharmaceutical substances. Mushrooms have been used in health care for treating simple and common diseases, like skin diseases and pandemic diseases like AIDS.

mushroom prebiotics gut microbiota anti-diabetic anti-cancer

1. Introduction

For countless ailments mushrooms have been used for several thousands of years. Initially, mushrooms were known to be only a source of food but, later, their medicinal properties were discovered ^[1]. The use of mushrooms dates back to the ancient Egyptians and ancient Chinese cultures to promote general health and longevity. The early record of the Materia Medica shows evidence of using mushrooms for treating diseases. The number of mushrooms identified to date represents only 10% of total mushrooms assumed to exist ^[2]. Mushrooms rich in polysaccharides, especially β glucans, can stimulate the immune system and provide the beneficial properties to medicinal mushrooms when compared to the other mushrooms. Mushrooms have high protein content (up to 44.93%), vitamins, fibers, minerals, trace elements, and low calories and they lack cholesterol ^[3]. Mushrooms offer significant vital health benefits, including antioxidants, cholesterol-lowering properties, anti-hypertensive, anti-inflammatory, liver protection, as well as anti-diabetic, anti-viral, and anti-microbial properties.

The prebiotics depress endogenous pathogens found within the gastrointestinal (GI) tract, allowing increased competency of the immune system to resist exogenous pathogens ^[4]. Prebiotics are food ingredients (such as mushroom) that can stimulate the growth of beneficial microbiota. Oligosaccharides and fibers are the major constituents of prebiotics. The recent trend in food science and technology has shown the association of prebiotics to modulate the human gut microbiota and attenuate several disease conditions such as diabetes, obesity, and cancer. The important sources of prebiotics in mushrooms are non-digestible mushroom polysaccharides which can inhibit pathogen proliferation by enhancing the growth of probiotic bacteria in the gut ^[5]. The gut microbiota can contribute to the onset of several metabolic dysregulations, leading to inflammation in the intestine, liver, and brain. Microbiota also regulates the energy metabolism ^[6].

2. Composition of Mushrooms

Mushrooms contain bioactive polysaccharides and essential amino acids, as well as minerals, such as such as calcium, potassium, magnesium, iron, and zinc. An interesting study revealed that the protein content in dry mushrooms was 228 and 249 g/kg dry matter (DM) ^[7]. Another important constituent of the mushrooms are carbohydrates, which constitute about one-half of mushroom DM. Carbohydrates play a significant role in the medicinal properties of mushrooms through their immune-stimulating β glucans, along with other polysaccharides ^[8]. Compared with the protein and carbohydrate contents, contents of total lipids (crude fat) are low, ranging mostly from 20 to 30 g/kg DM. Mushrooms contain various elements, in particular, potassium as the prevailing element. The compositions of many trace elements vary widely among species. The normal content of ascorbic acid is 150–300 mg/kg DM. B-group vitamin contents of thiamine (1.7–6.3 mg/kg), riboflavin (2.6–9.0 mg/kg), pyridoxine (1.4–5.6 mg/kg), and niacin (63.8–83.7 mg/kg) were determined in four dried common cultivated species. The average ergosterol content was 1.98 mg/g, the average vitamin D₂ content was 16.88 µg/g, and vitamin B2 content was 12.68 µg/g in 35 different mushrooms. In addition, vitamin D₂ content was increased in mushrooms followed by ultraviolet-C (UV-C) radiation ^[9]. There exists a consensus that phenolics—in particular, phenolic acids—are the major active component in mushroom. Phenolic acids can be divided into two major groups: hydroxy derivatives of benzoic acid and trans-cinnamic acid. Within the former group, protocatechuic, gentisic, p-hydroxybenzoic, gallic, vanillic, and syringic acids have usually been detected in mushrooms ^[10]. An interesting study on edible mushrooms commonly consumed in China revealed that mushrooms possess substantial antioxidant activity and the strongest metal chelating ability by virtue of their phenolic composition, in particular, gallic acid ^[11].

3. Medicinal Properties of Mushroom

Mushrooms are significant as a medicinal food. In fact, many mushrooms have long been used throughout Asia for medicinal purposes. Mushrooms possess antioxidant activity, anti-hypertensive activity, hypocholesterolemic activity, liver protection, as well as anti-inflammatory activity, anti-diabetic activity, anti-viral activity, and anti-microbial activity ^[12]. The researchers are going to discuss some of the common mushrooms with medicinal properties and proven to be beneficial for improving health status (Table 1).

Table 1. List of important medicinal mushrooms and their pharmacological benefits.

Medicinal Mushroom	Active Immunomodulators	Health Benefits	Gut Microbiota Regulation
Grifola frondosa	MD-fraction Grifolan	The Agaricus blazei-based mushroom extract, andosan, protects against intestinal tumorigenesis in A/J Min/+ mice ^[13].	Andosan may also have influenced the composition and activity of microbiota in the A/J Min/+ mice.
Pleurotus tuberregium	Polysaccharides	Pleurotus tuberregium possesses antihyperglycemic properties and attenuated oxidative stress in diabetic rats on a high-fat diet ^[14].	There are possible roles of gut microbiota in the polysaccharide-induced attenuation of obesity and hyperglycemia.
Ganoderma lucidum	GLP(AI), Ganopoly, Ganoderans	Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota ^[15].	GL has decreased Firmicutes-to-Bacteroidetes ratios. Reduced endotoxin-bearing Proteobacteria levels. It also maintains intestinal barrier integrity and reduces metabolic endotoxemia.
Polyporus umbellatus	Polysaccharides	Integrative fungal solutions for protecting bees ^[16].	Increases the intestinal microbiome to regulate host health.
Phellinus linteus	Polysaccharides	Anti-diabetic potential ^[17].	Phellinus linteus induces changes in the composition and activity of the gastrointestinal tract microbiota that confer nutritional and health benefits to the host.
Trametes versicolor	Krestin (PSK), PSP	Prevents host from diarrhea, Clostridium difficile infection, and inflammatory bowel disease ^[18].	Polysaccharopeptide from Trametes versicolor regulates the gut microbiota to maintain the host health.
Hericum erinaceus	Galactoxyloglucan–protein complex	Hericum erinaceus possesses anti-cancer, immuno-modulating, hypolipidemic, antioxidant and neuro-protective activities ^[19].	Hericum erinaceus renders changes in the composition and activity of the gastrointestinal tract microbiota that confer nutritional and health benefits to the host.
Agaricus bisporus	Polysaccharides	Anti-bacterial property ^[20].	White button mushrooms increase microbial diversity and accelerate the resolution of citrobacter rodentium infection in mice.
Fomitopsis officinalis	Polysaccharides	Fomitopsis officinalis acts as an insulin sensitizer in glucose tolerance tests and regulates hyperglycemia in mice with non-insulin-dependent diabetes ^[21].	Exact action on gut microbiota is yet to be discovered.
Lentinula edodes	Lentinan, KS-2	Lentinula edodes-derived polysaccharide rejuvenates mice in terms of immune responses and gut microbiota ^[22].	L2 reverses the gut microbiota structure, such as the reduced ratio Firmicutes/Bacteroidetes, the increased Bacteroidia, the decreased Bacilli and Betaproteobacteria, the increased Bacteroidaceae, the decreased Lactobacillaceae, and Alcaligenaceae.
Fomes fomentarius	Polysaccharides	Fomes fomentarius is used to cure various ailments such as dysmenorrhoea, hemorrhoids, bladder disorders, pyretic diseases, treatment of coughs, cancer, and rheumatism ^[23].	The exact role in regulating gut microbiota is not yet elucidated well.
Schizophyllum commune	Schizophyllan, Sonifilan, SPG	Used as an immune modulator ^[24].	The exact role in regulating gut microbiota is not yet elucidated well.

4. Gut Microbiota-Associated Health Benefits

Human gut microbiota contains more than ten trillion microorganisms, with 1000 species of known bacteria, with more than 3 million genes (150 times more than human genes) ^[25]. The human gut microbiota has become the subject of extensive research in recent years and our knowledge of the inhabitant species and its functioning increased ^[26]. The normal human gut microbiota comprises two major phyla, namely Bacteroidetes and Firmicutes. The microbiota of the gut helps to digest the foods which cannot be digested by stomach and intestine enzymes. It plays an important role in the immune system, performing a barrier effect. Gut barrier function is defined as the ability of the gut to protect the gut from harmful substances and control the intake across the mucosa. The barrier function is classified into physical (mucous layer, intestinal epithelial cells), chemical (gastric acid, digestive enzyme, and bile acid), biological (lymphocytes and immunoglobulin A), and immunological barriers (intestinal flora). It helps with the production of some vitamins (B and K). A regular healthy balanced diet has been shown to maintain a stable and healthy gut microbiota and reduce the risk of numerous diseases ^[27]. The gut microbiota largely derives their nutrients from dietary carbohydrates. The link between diet, gut microbiota, and health has been elegantly shown in animal models ^[28]. Animal diets changed from low fat/fiber rich plant diets to high fat/high sugar diets showed a significant decrease in Bacteroidetes phylum with an increase in Bacilli and Erysipelotrichi from the Firmicutes phylum ^[29].

There are many recent studies focusing on health benefits of gut microbiota; for example, a study reveals that prebiotics can regulate the gut microbiota plays a significant role in regulating non-alcoholic fatty liver disease (NAFLD) ^[30]. A recent study shows that the gut microbiota plays a protective role in the host defense against pneumococcal pneumonia ^[31]. Generally, the microbiota can be activated in favor of host health by various factors, such as probiotics (indicating microorganisms stimulate microbiota), prebiotics (food compounds rich in oligosaccharides or polysaccharides), and synbiotics (a combination of probiotics and prebiotics). Prebiotics research is of vital significance in studying the health benefits of gut microbiota ^[32].

Gut microbiota performs several functions which proven to be beneficial to the host including following aspects.

Metabolism of various nutrients: members of the genus Bacteroides, known to be a cardinal organism that interferes with carbohydrate metabolism—perform this by expressing enzymes such as glycoside hydrolases, glycosyl transferases, and polysaccharide lyases. The gut microbiota has also been shown to impart a positive impact on lipid metabolism by suppressing the inhibition of lipoprotein lipase activity in adipocytes ^[33]. The gut microbiota is rich in protein-metabolizing enzymes that function via the microbial proteinases and peptidases in tandem with human proteinases. Another major metabolic function of the gut microbiota is the synthesis of vitamin K and several components of vitamin B ^[34].

Drug metabolism: the importance of the gut microbiome in determining not only overall health, but also in the metabolism of drugs and xenobiotics, is rapidly emerging. Intestinal microbiota-mediated drug and toxicant metabolism is an unexplored ^[35], but vital, field of study in pharmacology and toxicology.

Regulation of immune system: the gut microbiota contributes to gut immunomodulation in tandem with both the innate and adaptive immune systems ^[36]. During the prolonged co-evolution, bacteria and its host developed some interactions governed by the host immune system. In response to intestinal bacteria or their metabolites, a variety of innate immune cells promotes or suppresses T cell differentiation and activation ^[37]. Some commensal bacteria or bacterial metabolites enhance or repress host immunity by inducing regulatory T cells. The intestinal epithelial cells between host immune cells and intestinal microbiota contribute to the separation of these populations and modulate host immune responses to intestinal microbiota ^[38].

5. Role of Mushrooms as Prebiotics in Improving the Host’s Health

Prebiotics are substances that induce the growth or action of microorganisms (e.g., bacteria and fungi) that contribute to the well-being of their host ^[39]. Prebiotics are identified based on the composition of fibers in them. Some of the commonly-known prebiotic foods are as follows: raw chicory root (64.6%), raw Jerusalem artichoke (31.5%), raw dandelion greens (24.3%), raw garlic (17.5%), and raw onion (8.6%). Apart from those mentioned above, mushrooms are also considered a potential source of prebiotics as they contain different polysaccharides, such as chitin, hemicellulose, mannans, α- and β-glucans, galactans, and xylans ^[40]. Mushrooms were found to play a vital role in immunoregulating pneumococcal pneumonia, atherosclerosis, and antitumor activities. In a recent study, researchers have found that white button mushrooms (WB mushrooms) increase microbial diversity and accelerate the resolution of Citrobacter rodentium infection in mice ^[20]. Specifically, WB mushrooms were reported to stimulate a local inflammatory response, the production of catecholamines, and their metabolites, and changed the composition of the gut flora. The results of their study provide information on biological changes that occur upon WB ingestion are likely to include direct stimulation of the innate immune systems that produce inflammation and affect the composition of the gut flora which improves GI health by limiting the damage that occurs following injury or infection. Another interesting study provides evidence for hypocholesterolemia properties and prebiotic effects of Mexican Ganoderma lucidum in C57BL/6 mice. In brief, the study explains significant reduction in lipogenic gene expression (Hmgcr, Fasn, Srebp1c, and Acaca) and genes responsible for reverse cholesterol transport (Abcg5 and Abcg8), as well as an increase in Ldlr gene expression in the liver and delineate a new source of bioactive compounds with hypocholesterolemic and prebiotic effects ^[41].

Ganoderma lucidium (GL) is a frequently mentioned mushroom that has been reported to reduce obesity in mice by modulating the composition of gut microbiota. GL reduces body weight, inflammation, and insulin resistance in mice fed a high-fat diet. The GL not only reverses gut dysbiosis—as indicated by the reduced Firmicutes/Bacteroidetes ratios and endotoxin-bearing Proteobacteria levels—but also alters the intestinal barrier probity and attenuates endotoxemia. The results confirm that GL can be used as a prebiotic agent to prevent gut dysbiosis and obesity-related metabolic disorders in obese individuals. Mushrooms are shown to improve the antioxidant status via microbiome alterations. The consumption of Agaricus bisporus mushroom affects the intestinal microbiota composition, performance, and morphology, and antioxidant levels of turkey poults. The results of this study state that A. bisporus is able to improve both growth performance and antioxidant activity of turkey poults and it also significantly increased the numbers of lactic acid-producing bacteria and improved the condition of the intestine ^[42].

Mushroom polysaccharides have been suggested to be potential prebiotics. Lentinula edodes-derived polysaccharide rejuvenates mice in terms of immune responses and gut microbiota. L2 reverses the gut microbiota structure, such as the reduced ratio Firmicutes/Bacteroidetes, the increased Bacteroidia, the decreased Bacilli and Betaproteobacteria, the increased Bacteroidaceae, the decreased Lactobacillaceae, and Alcaligenaceae. Phellinus linteus has been proved to have anti-tumor properties on skin, lung, and prostate cancer cells. Phellinus linteus induces changes in the composition and activity of the gastrointestinal tract microbiota that confer nutritional and health benefits to the host. The Trametes versicolor is a polypore mushroom. Polysaccharopeptide from Trametes versicolor regulates the gut microbiota to maintain the host health. Hericium erinaceus is a Chinese mushroom with nootropic properties that is also known as Lion’s Mane. H. erinaceus renders changes in the composition and activity of the gastrointestinal tract microbiota that confer nutritional and health benefits to the host.

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