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Abstract

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. This review is aimed at accumulating the health-promoting benefits of edible mushrooms through gut microbiota. Mushrooms are proven to possess anti-allergic, anti-cholesterol, anti-tumor, and anti-cancer properties. Mushrooms are rich in carbohydrates, like chitin, hemicellulose, β and α-glucans, mannans, xylans, and galactans, which make them the right choice for prebiotics. Mushrooms act as a prebiotics to stimulate the growth of gut microbiota, conferring health benefits to the host. In the present review, we have summarized the beneficial activities of various mushrooms on gut microbiota via the inhibition of exogenous pathogens and, thus, improving the host health.
International Journal of
Molecular Sciences
Review
A Critical Review on Health Promoting Benefits of
Edible Mushrooms through Gut Microbiota
Muthukumaran Jayachandran 1, Jianbo Xiao 2, * and Baojun Xu 1, *ID
1Programme of Food Science and Technology, Division of Science and Technology,
Beijing Normal University–Hong Kong Baptist University United International College,
No. 28 Jinfeng Road, Tangjiawan, Zhuhai 519085, Guangdong, China; jmkbio@uic.edu.hk
2State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences,
University of Macau, Macau, China
*Correspondence: JianboXiao@umac.mo (J.X.); baojunxu@uic.edu.hk (B.X.); Tel.: +86-75-6362-0636 (B.X.)
Received: 10 July 2017; Accepted: 5 September 2017; Published: 8 September 2017
Abstract:
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. This review
is aimed at accumulating the health-promoting benefits of edible mushrooms through gut microbiota.
Mushrooms are proven to possess anti-allergic, anti-cholesterol, anti-tumor, and anti-cancer properties.
Mushrooms are rich in carbohydrates, like chitin, hemicellulose,
β
and
α
-glucans, mannans, xylans,
and galactans, which make them the right choice for prebiotics. Mushrooms act as a prebiotics
to stimulate the growth of gut microbiota, conferring health benefits to the host. In the present
review, we have summarized the beneficial activities of various mushrooms on gut microbiota via
the inhibition of exogenous pathogens and, thus, improving the host health.
Keywords: 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
Int. J. Mol. Sci. 2017,18, 1934; doi:10.3390/ijms18091934 www.mdpi.com/journal/ijms
Int. J. Mol. Sci. 2017,18, 1934 2 of 12
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
D
2
content was 16.88
µ
g/g, and vitamin B2 content was 12.68
µ
g/g in 35 different mushrooms.
In addition, vitamin D
2
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
]. We are going to
discuss some of the common mushrooms with medicinal properties and proven to be beneficial for
improving health status (Table 1).
3.1. Ganoderma
Reishi is an edible medicinal mushroom that has been used for various healing abilities for several
decades; it possesses a strong anti-inflammatory function and is tied to longevity, better immune
function, and mental clarity [
13
]. It is generally referred as the king of mushrooms. The common
genus of this mushroom is Ganoderma and closely-related species include
Ganoderma lucidum
,G. tsugae,
and G. lingzhi. The total triterpenes in G. lucidum induce apoptosis in MCF-7 cells and attenuate
Dimethylbenz[a]anthracene (DMBA) induced mammary and skin carcinomas in experimental
animals [
14
]. G. lucidum polysaccharides also protect fibroblasts against UVB-induced photoaging [
15
].
G. lucidum also showed strong anti-inflammatory activity and it acted as an immunomodulator in
inflammation induced by a high-cholesterol diet [
16
]. The recent advancement in research has shown
the link between gut microbiota and treatment of various ailments. The constituents of the G. lucidum
make it one of the important prebiotics used to increase the bacterial flora. In particular it is rich
in polysaccharides, terpenoids, and total phenols. The prebiotic action of G. lucidum should be
due to the presence of several polysaccharides; a recent study has isolated the high and intermediate
Int. J. Mol. Sci. 2017,18, 1934 3 of 12
polysaccharides and shown to be responsible for its prebiotic action. The specific type of polysaccharide
present is the
β
-D-glucan polysaccharide. There are several types of polysaccharides present in
Ganoderma lucidium polysaccharides A, B, and C in a ratio of 2.5:72.5:25. The chief sugars found
in polysaccharides are rhamnose, D-galactose, and glucose and galactose. Ganoderma also contains
water-soluble polysaccharides with anti-tumor properties. Polysaccharides BN3C, 4 (glucose and
arabinose at molar ratio of 4:1) found in Ganoderma can boost and synthesize the metabolism of nucleic
acid protein. The polysaccharides, G-I (
β
-D-glucan) and GL-1, for example, have both been shown to
inhibit sarcoma. A fermentation study has found that fermentation of Ganoderma lucidum extracts have
shown prebiotic ability of polysaccharides in increasing the number of Bifidobacteria. The potential
prebiotic effect of the G. lucidum extract in batch-culture fermentation based on increments in the
growth of bacteria used (0.4–1.5 log10 CFU/mL) after 18 h of fermentation [
17
]. Supplementation of G.
lucidum polysaccharide strain S
3
(GLPS
3
) increased the relative abundance of the beneficial bacteria
such as lactobacillus,roseburia, and lachnospiraceae [
18
]. GLPS
3
inhibits pancreatitis through microbiota
regulation. In a similar way, two other species of reishi mushroom possess several pharmacological
properties, including antioxidant [
19
], antitumor [
20
], and hepatoprotective activities [
21
]. In an
interesting study ethanolic extract of G. lucidum showed an appreciable amount of antioxidant
compounds and also good free radical scavenging effects of different free radicals. The study shows
that G. lucidum compounds can be better antioxidant supplements for nutrients [
22
]. This may be due
to the rich phenolic contents of G. lucidum.
3.2. Chaga Mushroom
Chaga mushroom is another promising candidate in the field of medicinal mushrooms. The major
constituents are betulinic acid derivatives and melano-glucan complexes, and chaga have traditionally
been boiled to make a tea, which is drunk to treat a range of conditions, including cancers, viral
and bacterial infections, and gastro-intestinal disorders [
23
,
24
]. Inonotus obliquus belongs to higher
basidiomycetes of chaga medicinal mushrooms. Inonotus obliquus presented protective effects against
the oxidative stress in liver induced by tert-butyl hydroperoxide in primary-cultured rat hepatocytes.
The above said property maybe due to its ability to scavenge the free radicals and thereby it inhibits
the leakage of liver marker enzymes as a result of liver damage [
25
]. The high total phenolic contents
maybe the reason for its strong antioxidant activity. Like several other mushrooms, I. obliquus also
possesses anti-cancer activity. The ergosterol peroxide from I. obliquus exhibits anti-cancer activity by
down-regulation of the
β
-catenin pathway in colorectal cancer and it shows that it down-regulated
β
-catenin signaling, which exerted anti-proliferative and pro-apoptotic activities in colorectal cancer
(CRC) cells. This proves that I. obliquus can be developed as promising medicine to treat colon
cancer [
26
]. With context to this; another study shows that ethanolic extract of Innotus obliquus
induces G1 cell cycle arrest in HT-29 human colon cancer cells [
27
]. The biological activity of the
Inonotus obliquus is mainly due to the presence of several polysaccharides, the polysaccharides of
Inonotus obliquus mainly constitutes the following sugars: rhamnose, arabinose, xylose, mannose,
glucose, and galactose. An interesting study finds that Inonotus obliquus polysaccharide (IOP)
contains polysaccharide content of 98.6%, and Man, Rha, Glu, Gal, Xyl, and Ara in a ratio of
9.8:13.6:29.1:20.5:21.6:5.4 as monosaccharide. The study reveals that IOP induce changes in the gut
microbiota and increased the Bacteroidetes at the phylum level, and brings the changes towards a
healthy bacterial profile. The experiment was carried with three different doses of IOP 0.1, 0.2, and
0.4 g/kg/day. The result of the study states that the predominant phylum was Bacteroidetes, normal
control (NC) shows 65.05%, 47.47% in model control (MC) group. The composition of Bacteroidetes was
increased about 4.55%, 9.56%, 17.48%, and 20.81% in IOP-L, IOP-M, IOP-H, and Qingyilidan granule
treated (PC) groups, respectively. The PC group (Qingyilidan granule) is the standard compared with
the three different doses of IOP [28].
Int. J. Mol. Sci. 2017,18, 1934 4 of 12
3.3. Coriolus versicolor
Like other mushrooms, Coriolus is also rich in polysaccharides and used as traditional
medicine to treat cancer, AIDS, and some fungal infections. C. versicolor shows
in vivo
and
in vitro
anti-tumor and anti-metastasis effects on mouse mammary 4T1 carcinoma [
29
]. A remarkable
immunomodulatory effect was reflected by the augmentation of IL-2, 6, 12, Tumor necrosis
factor-
α
(TNF-
α
), and interferon-gamma (IFN-
γ
) productions from the spleen lymphocytes of C.
versicolor-treated tumor-bearing mice. Ternatin, a cyclic peptide isolated from corioulus versicolor,
and its derivative found to suppress hyperglycemia and hepatic fatty acid synthesis in diabetic Kuo
Kondo yellow obese (KK-A(y)) mice. The main finding of this study proves that C. versicolor has
lowered glucose, and triglycerides significantly (p< 0.05) and Sterol regulatory element-binding
protein-1c (SREBP-1c) mRNA level in hepatoma 1-6 (Hepa1-6) hepatocyte cells was reduced, but
not significantly [
30
]. The SREBP-1c is an insulin-dependent molecule that regulates de novo
lipogenesis.The positive regulation on the SREBP-1c can directly regulates hyperglycemia and fatty
acid synthesis via insulin signaling. Polysaccharopeptide (PSP) is the polysaccharide present in Coriolus
versicolor. It is a heteropolysaccharide with
β
-1,3-glucan with
β
-1,6 branches. The previous study has
also reported that PSP modified Bifidobacterium spp. and Lactobacillus spp. and by that it regulates the
human microbiome [
31
]. Another study also reported that polysaccharopeptide (PSP) from Trametes
versicolor can alter the bacterial flora. In this experiment they have healthy human for a clinical trial.
In PSP group provided 1200 mg, three times daily on an empty stomach during days 1 to 14. The results
of the study states that PSP regulated microbiome composition by eliciting host responses that, in turn,
regulated the microbiome [
32
]. A recent study showed the chemical analyses of Coriolus versicolor
extract revealed a high amount of total phenolics in C. versicolor, 25.8
±
1.4 mg
·
g
1
[
33
]. It also shows
a strong antioxidant activity in the experiment.
3.4. Maitake
Maitake with polysaccharides as principle constituents has been reported to strongly interact
with the immune system. The mushroom Grifola frondosa contains starch, natural oligofructoses,
fructo-oligosacharides (FOS), lactulose, galactomannan, and indigestible polydextrose, indigestible
dextrin and
β
-glucan. Grifola frondosa is a species of maitake and its D-fraction is rich in proteoglucan,
which has long been exclusively attributed to their immune-stimulatory capacity. In particular,
it decreases cell viability, increases cell adhesion, and reduces the migration and invasion of mammary
tumor cells, generating a less aggressive cell behavior in a murine model of breast cancer [
34
].
G. frondosa also inhibits hepatocellular carcinoma by inhibiting proliferation, inducing cell cycle
arrest, and inducing apoptosis in Hep3B hepatoma cells [
35
]. G. frondosa also shows anti-cancer
activity on B16 melanoma cells [
36
]. Cordyceps is an important mushroom of this group can benefit via
metabolic efficiency increase (fat metabolism) and helps to prevent the host from viral infections by its
ability to synthesize nucleoside derivatives.
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) [
37
]. 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 [
38
]. 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
Int. J. Mol. Sci. 2017,18, 1934 5 of 12
(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 [
39
]. 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 [
40
]. 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 [41].
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) [
42
]. A recent study shows that the gut microbiota plays a
protective role in the host defense against pneumococcal pneumonia [
43
]. 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 [44].
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 [
45
]. 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 [46].
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 [
47
], 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 [
48
]. 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 [
49
]. 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 [50].
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 [
51
]. 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 [
52
]. 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 [
53
].
Specifically, WB mushrooms were reported to stimulate a local inflammatory response, the production
Int. J. Mol. Sci. 2017,18, 1934 6 of 12
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 [54].
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 [55].
Gut microbiota composition has been reported to alter the gut barrier, affect adipose tissue
proliferation, and affect energy metabolism, all of which can be changed through the use of
prebiotics [
56
]. Lentinula edodes-derived polysaccharide alters the spatial structure of gut microbiota
in mice; in brief L2 treatment decreased the gut microbiota’s diversity and evenness in the intestine,
particularly in the colon and cecum [
57
]. Other populations also changed in response to L2 treatment
include Proteobacteria, Acidifaciens, Bacteroides,Helicobacter suncus, and Alistipes. Recently some
researchers have evaluated the prebiotic properties of edible mushrooms, the selected mushrooms;
Pleurotus ostreatus,P. sajor-caju, and P. abalonus represent the bifidogenic effect which can stimulate
the growths of Bifidobacterium bifidum TISTR 2129, B. breve TISTR 2130, B. animalis TISTR 2195, and
B. longum TISTR 2194 [
58
]. This study acknowledges that these mushrooms should be studied in
future for their assistance in improving hosts health via its prebiotic properties. It is evident that in the
above studies that mushroom can act as potential prebiotics to improve the microbiome in favor of
host health. There are about 380 or more species of mushrooms that are proven to possess medicinal
properties, so a large number of prebiotic sources may be encountered in the future.
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.
Int. J. Mol. Sci. 2017,18, 1934 7 of 12
6. Conclusions and Future Perspectives
The traditional medicinal system has used foods as medicines; one such kind of traditional remedy
commonly used consists of mushrooms with medicinal properties. There are several edible mushrooms
that have significant medicinal metabolites. These mushrooms can make better prebiotics to stimulate
the gut microbiota. There are several sources of various prebiotics, such as seaweed, but mushrooms
have the advantage of their easy availability and having been studied extensively, when compared
to other prebiotics. Mushrooms contain various active polysaccharides and phenolic compounds
make it biologically valuable. The gut microbiota comprises of trillions of bacteria that contribute to
the nutrient acquisition and energy regulation [
59
]. The microorganisms present in the gut play an
important role in the health of the digestive system, and also have an influence on the immune system.
The immune tissues in the gastrointestinal tract constitute the largest and most complex fraction of the
human immune system [
60
]. We saw earlier that gut microbiota plays an important role in various
factors such as physiology, organ development, and aging. We have also discussed the beneficial
effects of gut microbiota in various pathological conditions. The medicinal mushrooms can act as
immunomodulatory agents to activate gut microbiota. The current review discusses the important
areas in mushrooms regulated gut microbiota in the host’s health. We have discussed different
mushrooms, their composition, and pharmacological properties, such as antioxidant, hypolipidemic,
and atherosclerosis capabilities. We have also discussed some recent research studying the roles of
mushrooms in regulating gut microbiota and the mechanism by which mushrooms regulate the gut
microbiota. The exact role of the active constituents of some mushrooms are not yet documented
and, in the future, a detailed research on the same would add more knowledge to the existing idea
regarding the role of mushrooms in gut microbiota regulation and imparting health benefits.
As we saw earlier, microbiota play a significant role in human health and disease; often they are
referred to as the “forgotten organ”. So far the research on the regulation of microbiota by various
mushrooms has been insufficiently studied. Future studies on gut microbiota studies may include
(1) analysis of functional composition of beneficial gut microbiota; (2) the genomic analysis of the
gut microbiota and the changes happened at the genetic level of the microbiota upon the mushroom
feeding (metagenomics or ecogenomics); (3) the exact mechanism by how the change in the microbial
population affects the pathological conditions; (4) detailed study on the immune interaction of the host
with the microbiota; (5) the role of mushrooms in balancing the microbiota to maintain the healthy
host; (6) the pharmacokinetics and drug toxicity of the medicines should be studied for the effects of
microbiome on it; (7) analysis of the microbial population in the early and later pathological stages; and
(8) characterization of the global microbiota and how the different diets affect the microbial community.
Apart from all the above directions researchers are also interested in studies related to restoring the
microbial balance. An interesting study has found that donating the healthy microbiota from a donor
to the host affected by Clostridium difficile-associated disease (CDAD) can improve the health condition.
Treatment for two weeks significantly prevented the dysbiosis and the symptoms associated with
CDAD were found to have disappeared [
61
]. Even though they achieved the beneficial effects, the
host-donor compatibility and the critical risks pre- and post-transplantation of microbiota still remains
unclear. This needs to be studied extensively in order to derive a proper conclusion. Overall we
have summarized the updated research in the field of prebiotic-induced gut microbiota and its health
benefits. The results from the above said directions may open up a great field of disease management.
Int. J. Mol. Sci. 2017,18, 1934 8 of 12
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 [62].
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 [63].
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 [64].
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 [65]. Increases the intestinal microbiome to regulate host health.
Phellinus linteus Polysaccharides Anti-diabetic potential [66].
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 [32].
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 [67].
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 [53].
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 [68].
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 [69].
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
[70].
The exact role in regulating gut microbiota is not yet elucidated well.
Schizophyllum commune
Schizophyllan, Sonifilan, SPG
Used as an immune modulator [71].
The exact role in regulating gut microbiota is not yet elucidated well.
Int. J. Mol. Sci. 2017,18, 1934 9 of 12
Acknowledgments:
The authors thank Beijing Normal University–Hong Kong Baptist University United
International College, Zhuhai, Guangdong, China for data collection and providing a space to prepare the
review. The work was funded by grants UIC 201627 and UIC 201714 from the Beijing Normal University–Hong
Kong Baptist University United International College, Zhuhai, Guangdong, China.
Author Contributions:
Muthukumaran Jayachandran and Baojun Xu have designed the concept, organized the
writing, and proofread the review, and Jianbo Xiao has edited and proofread the review.
Conflicts of Interest: The authors declare no conflict of interest.
Abbreviations
DM Diabetes Mellitus
UV-C Ultraviolet-C
DMBA Dimethylbenzanthracene
MCF-7 Michigan Cancer Foundation-7 Cells
GLPS3 G. lucidum Polysaccharide Strain S3
IL-2 Interleukin-2
TNF-αTumor Necrosis Factor- α
IFN-γInterferon-γ
NAFLD Non-Alcoholic Fatty Liver Disease
GI Gastrointestinal
WB mushroom White Button Mushroom
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2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
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(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
... It therefore acts as first barrier against pathogens and elicits immune responses. The immune system then functions by initiating the innate and adaptive immunity (Jayachandran et al., 2017). Various bioactive molecules of mushrooms and their targets/mechanism of action are listed in table 2. ...
... It acts as a barrier and does protection of the gut from harmful substances. The gut microbiome mainly digests carbohydrates derived from diet and they flourish (Jayachandran et al., 2017). Study reveals the regulation of gut microbiota is through prebiotics in non-alcoholic fatty liver diseases (NAFLD) (Clarke et al., 2012). ...
... The gut microbiota results in the activation of immune system upon the foreign substance invasion. Coevolution suggests that evolution of bacteria and its host is relative to host-immune system in a way that host bacteria interaction surveillance is done by host-immune system (Jayachandran et al., 2017). ...
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Well-characterized and standardized extracts of a Mexican genotype of Ganoderma lucidum (Gl), a medicinal mushroom, cultivated on oak sawdust (Gl-1) or oak sawdust plus acetylsalicylic acid (Gl-2, ASA), have been shown to exert antioxidant, hypocholesterolemic, anti-inflammatory, prebiotic, and anticancer properties. However, toxicity analyses still need to be carried out. Different doses of these Gl-1 or Gl-2 extracts were administered to Wistar rats for 14 days in a repeated dose oral toxicity study. We assessed the external clinical signs, biochemical parameters, liver and kidney tissues, injury and inflammation biomarkers, gene expression, inflammatory responses, proinflammatory mediators, and gut microbiota. Gl extracts had no significant adverse, toxic or harmful effects on male and female rats compared to the control groups. No injury or dysfunction were recorded in the kidney or liver, as there were no significant abnormal variations in organ weight, tissue histopathology, serum biochemical parameters (C-reactive protein, creatinine, urea, glucose, ALT and AST transaminases, TC, LDL-c, TG, HDL-c), urinary parameters (creatinine, urea nitrogen, albumin, the albumin-to-creatinine ratio, glucose), injury and inflammatory biomarkers (KIM-1/TIM-1, TLR4, and NF-кB protein expression; IL-1β, TNF-α and IL-6 gene expression), or the expression of genes linked to cholesterol metabolism (HMG-CoA, Srebp2, Ldlr). Gl-1 and Gl-2 extracts showed prebiotic effects on the gut microbiota of male and female Wistar rats. Bacterial diversity and relative bacterial abundance (BRA) increased, positively modulating the Firmicutes/Bacteroidetes ratio. The ASA (10 mM) added to the substrate used for mushroom cultivation changed properties and effects of the Gl-2 extract on Wistar rats. The no-observed-adverse-effect-level (NOAEL) was 1000 mg/kg body weight/day of Gl-1 or Gl-2 extracts. Clinical trials are recommended for further exploring the potential therapeutic applications of studied extracts.
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Grifola frondosa (GF) is an edible mushroom with hypoglycemic and hypolipidemic effects. In this study, the specific pathogen-free male mice were randomized into the normal (NM), low-dose GF (LGF), medium-dose GF (MGF), and high-dose GF (HGF) groups. The LGF, MGF, and HGF groups were fed with 1.425 g/(kg d), 2.85 g/(kg d), and 5.735 g/(kg d) of GF solution for 8 weeks. After feeding with GF solution, compared with the NM group, the thymus index was significantly increased in the LGF group, and TC, TG, and LDL of mice were significantly increased in the HGF group, while HDL was significantly decreased. Compared with the NM group, the uncultured Bacteroidales bacterium, Ligilactobacillus increased in the LGF group, and Candidatus Arthromitus increased in the MGF group. The characteristic bacteria of the HGF group included Christensenellaceae R7, unclassified Clostridia UCG 014, unclassified Eubacteria coprostanoligenes, and Prevotellaceae Ga6A1. Among them, Ligilactobacillus showed a negative correlation with HDL. Unclassified Eubacterium coprostanoligenes group and Ligilactobacillus showed a positive correlation with TG. In summary, our experiments evidenced that GF improves lipid metabolism disorders by regulating the intestinal microbiota, providing a new pathway for hypolipidemic using GF dietary.
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Consumers are becoming aware of functional ingredients such as medicinal herbs, polyphenols, mushrooms, amino acids, proteins, and probiotics more than ever before. Like yogurt and its probiotics, L-glutamine, quercetin, slippery elm bark, marshmallow root, N-acetyl-D-glucosamine, licorice root, maitake mushrooms, and zinc orotate have demonstrated health benefits through gut microbiota. The impact of these ingredients on yogurt starter culture bacteria characteristics is not well known. The objective of this study was to determine the influence of these ingredients on the probiotic characteristics, tolerance to gastric juices and lysozyme, protease activity, and viability of Streptococcus thermophilus STI-06 and Lactobacillus bulgaricus LB-12. Acid tolerance was determined at 0, 30, 60, 90, and 120 min of incubation, whereas bile tolerance was analyzed at 0, 4, and 8 h. The microbial growth was determined at 0, 2, 4, 6, 8, 10, 12, 14, and 16 h of incubation, while protease activity was evaluated at 0, 12, and 24 h. The application of marshmallow root, licorice root, and slippery elm bark improved bile tolerance and acid tolerance of S. thermophilus. These ingredients did not impact the bile tolerance, acid tolerance, and simulated gastric juice tolerance characteristics of L. bulgaricus over 8 h and 120 min (respectively) of incubation. Similarly, the growth of S. thermophilus and L. bulgaricus was not affected by any of these functional ingredients. The application of marshmallow root, N-acetyl-D-glucosamine, and maitake mushroom significantly increased the protease activity of S. thermophilus, whereas the protease activity of L. bulgaricus was not affected by any ingredient. Compared to the control, marshmallow root and quercetin samples had higher mean log counts and log counts for S. thermophilus on the simulated gastric juice and lysozyme resistance in vitro test, respectively. For L. bulgaricus, licorice root, quercetin, marshmallow root, and slippery elm bark samples had higher log counts than the control samples.
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The antibacterial activity of methanol extract obtained from fruiting body of industrially grown basidiomycete Coriolus versicolor was examined. The Minimum Inhibitory Concentration (MIC) values against various bacteria ranged from 0.625 to 20 mg mL −1. C. versicolor expressed bactericidal activity against both Gram-positive and Gram-negative bacteria. The growth curves of Staphylococcus aureus and Salmonella enterica serovar Enteritidis, measured at 630 nm, and confirmed with macrodilution method showed that the obtained extract could inhibit the growth of tested bacteria. Scanning electron microscopy (SEM), transmission electron microscopy (TEM), and the loss of 260-nm-absorbing material were used to examine the ultrastructural changes in bacteria induced by the extract. When S. aureus was exposed to the MIC of C. versicolor, elongated and malformed cells were observed by SEM, while S. Enteritidis treated cells appeared shorter and aggregated with ruptured cell walls. TEM revealed the formation of non-membrane-enclosed bodies and depleted inner content of S. aureus. Larger and irregular periplasmic space and deformed and scattered components of the cell envelope were observed in treated S. Enteritidis. The loss of 260-nm-absorbing material indicated that the disruptive action of the extract on cytoplasmic membrane was more pronounced in S. aureus than in S. Enteritidis treated cells. The UV and FTIR spectrophotometric analyses revealed diverse composition of C. versicolor extract and high content of total phenolics. Altogether, mushroom extracts could be used to develop nutraceuticals or drugs effective against pathogenic microorganisms.
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Prebiotics are considering as non-digestible food ingredients which stimulate the growth of beneficial bacteria in the gastrointestinal tract. It mainly consists of the dietary fibers and oligosaccharides. They are having the beneficial effects like gut health maintenance, cancer inhibition, immunopotentiation, cholesterol removal, prevention of obesity. One of the potential sources of the prebiotics is mushroom polysaccharides. Mushroom fruiting body contains high amount of polysaccharides i.e. lentinan, β-1,3 glucan, β-1,6 glucan, grifolan and its showed multiple health benefits i.e. immunosuppressive, anticancer, hypertension, diabetes, stimulate the probiotics. Hence these fruiting bodies extracts extends their use for the human health.
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Background The novel A/J Min/+ mouse, which is a model for human Familial Adenomatous Polyposis (FAP), develops spontaneously multiple adenocarcinomas in the colon as well as in the small intestine. Agaricus blazei Murill (AbM) is an edible Basidiomycetes mushroom that has been used in traditional medicine against cancer and other diseases. The mushroom contains immunomodulating β-glucans and is shown to have antitumor effects in murine cancer models. Andosan™ is a water extract based on AbM (82%), but it also contains the medicinal Basidiomycetes mushrooms Hericeum erinaceus and Grifola frondosa. Methods and findings Tap water with 10% Andosan™ was provided as the only drinking water for 15 or 22 weeks to A/J Min/+ mice and A/J wild-type mice (one single-nucleotide polymorphism (SNP) difference), which then were exsanguinated and their intestines preserved in formaldehyde and the serum frozen. The intestines were examined blindly by microscopy and also stained for the tumor-associated protease, legumain. Serum cytokines (pro- and anti-inflammatory, Th1-, Th2 -and Th17 type) were measured by Luminex multiplex analysis. Andosan™ treated A/J Min/+ mice had a significantly lower number of adenocarcinomas in the intestines, as well as a 60% significantly reduced intestinal tumor load (number of tumors x size) compared to control. There was also reduced legumain expression in intestines from Andosan™ treated animals. Moreover, Andosan™ had a significant cytotoxic effect correlating with apoptosis on the human cancer colon cell line, Caco-2, in vitro. When examining serum from both A/J Min/+ and wild type mice, there was a significant increase in anti-tumor Th1 type and pro-inflammatory cytokines in the Andosan™ treated mice. Conclusions The results from this mouse model for colorectal cancer shows significant protection of orally administered Andosan™ against development of intestinal cancer. This is supported by the finding of less legumain in intestines of Andosan™ treated mice and increased systemic Th1 cytokine response. The mechanism is probably both immuno-modulatory and growth inhibition of tumor cells by induction of apoptosis.
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Ganoderma lucidum has featured in traditional Chinese medicine for >1,000 years. Ganoderma polysaccharides (GL-PS), a major active ingredient in Ganoderma, confer immune regulation, antitumor effects and significant antioxidant effects. The aim of the present study was to investigate the efficacy and mechanism of GL-PS-associated inhibition of ultraviolet B (UVB)-induced photoaging in human fibroblasts in vitro. Primary human skin fibroblasts were cultured, and a fibroblast photoaging model was built through exposure to UVB. Cell viability was measured by MTT assay. Aged cells were stained using a senescence-associated β-galactosidase staining (SA-β-gal) kit. ELISA kits were used to analyze matrix metalloproteinase (MMP)-1 and C-telopeptides of Type I collagen (CICP) protein levels in cellular supernatant. ROS levels were quantified by flow cytometry. Cells exposed to UVB had decreased cell viability, increased aged cells, decreased CICP protein expression, increased MMP-1 protein expression, and increased cellular ROS levels compared with non-exposed cells. However, cells exposed to UVB and treated with 10, 20 and 40 μg/ml GL-PS demonstrated increased cell viability, decreased aged cells, increased CICP protein expression, decreased MMP-1 protein expression, and decreased cellular ROS levels compared with UVB exposed/GL-PS untreated cells. These results demonstrate that GL-PS protects fibroblasts against photoaging by eliminating UVB-induced ROS. This finding indicates GL-PS treatment may serve as a novel strategy for antiphotoaging.
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D-Fraction is protein-bound β-1,6 and β-1,3 glucans (proteoglucan) extracted from the edible and medicinal mushroom Grifola frondosa (Maitake). The antitumoral effect of D-Fraction has long been exclusively attributed to their immunostimulatory capacity. However, in recent years increasing evidence showed that D-Fraction directly affects the viability of canine and human tumor cells, independent of the immune system. Previously, we have reported that D-Fraction modulates the expression of genes associated with cell proliferation, cell death, migration, invasion, and metastasis in MCF7 human breast cancer cells. Therefore, the purpose of the current study is to investigate if this modulation of gene expression by Maitake D-Fraction really modulates tumor progression. In the present work, we demonstrate for the first time that Maitake D-Fraction is able to act directly on mammary tumor cells, modulating different cellular processes involved in the development and progression of cancer. We demonstrate that D-Fraction decreases cell viability, increases cell adhesion, and reduces the migration and invasion of mammary tumor cells, generating a less aggressive cell behavior. In concordance with these results, we also demonstrate that D-Fraction decreases tumor burden and the number of lung metastases in a murine model of breast cancer.
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Most fatal mushroom poisonings are caused by species of the genus Amanita; the amatoxins are responsible for acute liver failure and death in humans. Ganoderma lucidum is a well-known traditional medicinal mushroom that has been shown to have obvious hepatoprotective effects. This study evaluated the hepatoprotective effects of triterpenoids from G. lucidum on liver injury induced by a-amanitin (a-AMA) in mice and the mechanisms of action of these triterpenoids, including radical scavenging and antiapoptosis activities. Mice were treated with a-AMA, followed by G. lucidum total triterpenoids or individual triterpenoids, and their hepatoprotective effects were compared with those of the reference drug silibinin (SIL). Treatment with SIL, G. lucidum total triterpenoids, and each of the 5 individual triterpenoids significantly reduced serum alanine aminotransaminase and aspartate ami-notransaminase concentrations and reduced mortality rates 20-40%. Moreover, triterpenoids and SIL significantly enhanced superoxide dismutase and catalase activity and reduced malondialdehyde content in livers. Treatment with ganoderic acid C2 significantly inhibited DNA fragmentation and decreased caspase-3, -8, and -9 activities. The results demonstrated that triterpenoids have hepatoprotective effects on a-AMA-induced liver injury and that their hepatoprotective mechanisms may be the result of their antioxidative and radical scavenging activities and their inhibition of apoptosis.
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Ganoderma lucidum total triterpenes were evaluated for its apoptosis-inducing and anti-cancer activities. Cytotoxicity and pro-apoptotic effect of total triterpenes were evaluated in human breast adenocarcinoma (MCF-7) cell line using MTT assay and flow cytometry. Total triterpenes induced apoptosis in MCF-7 cells by down-regulating the levels of cyclin D1, Bcl-2, Bcl-xL and also by up-regulating the levels of Bax and caspase-9. Anti-carcinogenicity of total triterpenes was analysed using dimethyl benz [a] anthracene (DMBA) induced skin papilloma and mammary adenocarcinoma in Swiss albino mice and Wistar rats respectively. Topical application of 5 mg, 10 mg and 20 mg total triterpenes reduced the incidence of skin papilloma by 62.5, 37.5 and 12.5% respectively. Incidence of the mammary tumour was also reduced significantly by 33.33, 66.67 and 16.67% in 10, 50 and 100 mg/kg b.wt. total triterpenes treated animals respectively. Total triterpenes were also found to reduce the average number of tumours per animal and extended the tumour latency period in both the models. The results indicate the potential cytotoxicity and anti-cancerous activity of total triterpenes, there by opens up a path to the development of a safe and successive chemo preventive agent of natural origin.
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Mushrooms are a great source of vitamin D and vitamin B2; however, the content of these vitamins in dried mushrooms has not fully been investigated. Thus, the objectives of this study were to determine the contents of vitamin D2, ergosterol, and vitamin B2 in commercially dried edible mushrooms in China and to investigate the effect of UV-C irradiation on fresh mushrooms. Among the 35 species of dried mushrooms considered for this study, the average ergosterol content was 1.98 mg/g, while the average vitamin D2 content was 16.88 µg/g. The average vitamin B2 content in dried mushrooms was 12.68 µg/g. Fresh shaggy ink caps and oyster mushrooms, when exposed to UV-C at 254 nm at a dose of 0.25 J/cm(2) for 10, 30, and 60 min, showed significantly (p < 0.05) increased vitamin D2 content (229.7 and 67.0 µg/g, respectively) as compared to its fresh counterparts. The conversion of ergosterol to vitamin D2 induced by UV-C irradiation at 0.25 J/cm(2) was significant (p < 0.05). In conclusion, dried commercial mushrooms have higher contents of ergosterol and vitamin D2 than fresh mushrooms. UV-C radiation can be used to increase vitamin D2 content in mushrooms.