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Biological activity and fatty acid composition of Caesar's mushroom

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Context: Due to its pleasant aroma and flavor, Amanita caesarea (Scop.) Pers. (Amanitaceae) has been a famous macrofungus since ancient times. This species is also well known in Turkey where people consume it extensively. Objective: Evaluation of the medicinal importance of A. caesarea for human health. Materials and methods: Antioxidant capacity of A. caesarea was studied using the methods of a scavenging effect on 2,2-diphenyl-1-picrylhydrazyl radicals, β-carotene-linoleic acid assay, reducing power and estimation of phenolics. Chloroform, acetone and methanol extracts of A. caesarea were tested for their antimicrobial activity against four Gram-positive bacteria, five Gram-negative bacteria and one yeast by applying a micro dilution method. The fatty acids were estimated via the method of gas chromatography analysis. Results: The scavenging effect of A. caesarea on DPPH radicals was measured as 40.91% at 0.5 mg/mL concentration, and its reducing power was 0.451 mg/mL at 1.2 mg/mL concentration. The phenolics found were catechin (32.5 mg/g), ferulic acid (7 mg/g), p-coumaric acid (6 mg/g) and cinnamic acid (6.2 mg/g). The highest minimum inhibitory concentration observed against the test microorganisms were with the acetone extract (4.8 µg/mL concentration) against Candida albicans. Thirty-seven different fatty acids were determined from A. caesarea, and oleic acid (58%) was the dominant component. Discussion and conclusion: Amanita caesarea had a high-antioxidant and -antimicrobial activity, and it also had important essential fatty acids required for human health. According to the results, this mushroom can be recommended as a major source of natural food.
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2013
http://informahealthcare.com/phb
ISSN 1388-0209 print/ISSN 1744-5116 online
Editor-in-Chief: John M. Pezzuto
Pharm Biol, 2013; 51(7): 863–871
!2013 Informa Healthcare USA, Inc. DOI: 10.3109/13880209.2013.768272
ORIGINAL ARTICLE
Biological activity and fatty acid composition of Caesar’s mushroom
Hasan Hu¨ seyin Dog
˘an and Gu¨ lsu¨ n Akbas¸
Biology Department, Science Faculty, Selcuk University, Campus, Konya, Turkey
Abstract
Context: Due to its pleasant aroma and flavor, Amanita caesarea (Scop.) Pers. (Amanitaceae) has
been a famous macrofungus since ancient times. This species is also well known in Turkey
where people consume it extensively.
Objective: Evaluation of the medicinal importance of A.caesarea for human health.
Materials and methods: Antioxidant capacity of A.caesarea was studied using the methods of a
scavenging effect on 2,2-diphenyl-1-picrylhydrazyl radicals, b-carotene–linoleic acid assay,
reducing power and estimation of phenolics. Chloroform, acetone and methanol extracts of
A.caesarea were tested for their antimicrobial activity against four Gram-positive bacteria, five
Gram-negative bacteria and one yeast by applying a micro dilution method. The fatty acids
were estimated via the method of gas chromatography analysis.
Results: The scavenging effect of A. caesarea on DPPH radicals was measured as 40.91% at
0.5 mg/mL concentration, and its reducing power was 0.451 mg/mL at 1.2 mg/mL concentra-
tion. The phenolics found were catechin (32.5 mg/g), ferulic acid (7 mg/g), p-coumaric acid
(6 mg/g) and cinnamic acid (6.2mg/g). The highest minimum inhibitory concentration observed
against the test microorganisms were with the acetone extract (4.8 mg/mL concentration)
against Candida albicans. Thirty-seven different fatty acids were determined from A.caesarea,
and oleic acid (58%) was the dominant component.
Discussion and conclusion:Amanita caesarea had a high-antioxidant and -antimicrobial activity,
and it also had important essential fatty acids required for human health. According to the
results, this mushroom can be recommended as a major source of natural food.
Keywords
Amanita caesarea, gas chromatography, Gram
positive and negative bacteria, HPLC, micro
dilution, phenolics, radical scavenging,
Turkey
History
Received 11 June 2012
Revised 1 November 2012
Accepted 16 January 2013
Published online 25 March 2013
Introduction
Fungi have been used as tea or nutritious food source in
Eastern cultures for many years because of their unique scents
and soft structures. Certain species of edible, inedible and
poisonous mushrooms are known in terms of significant
medicinal properties, and their extracts are also used for the
possible treatment of a number of diseases worldwide. Some
special species, such as Lentinula edodes (Berk.) Pegler
(shiitake) (Marasmiaceae), Grifola frondosa (Dicks.) Gray
(maitake) (Meripilaceae), Ganoderma lucidum (Curtis)
P.Karst. (mannentake) (Ganodermataceae) and Cordyceps
spp. (Cordycipitaceae), have a history of medicinal usage in
parts of Asia. The studies have indicated that mushrooms have
cardiovascular, anticancer, antiviral, antibacterial, anti-para-
sitic, anti-inflammatory, hepato-protective and glycemic
regulatory activities (Barros et al., 2007; Jua et al., 2010;
Yang et al., 2002).
Antioxidants, or the molecules that have a scavenging
effect on free radicals, are known as potentially protective
substances (Ramirez-Anguiano et al., 2007). This protective
effect is mainly attributed to well-known antioxidants such as
ascorbic acid, tocopherols and b-carotenes, but plant phenols
also play an important role.
Fatty acids are important constituents of fungal cells with
recognized roles as storage material, and as components of
plasmalemma and cell organelle membranes. In fungi, the
major fatty acids that typically occur in membrane phospho-
lipids and storage triacylglycerols are palmitic and stearic
acids, and their unsaturated derivatives palmitoleic, oleic,
linoleic and linolenic acids (Suutari, 1995). Mushrooms
reveal highly variable fatty acid profiles, and palmitic, oleic
and linoleic acids are the most abundant fatty acids found in
the members of Basidiomycetes. Interest in lipids, especially
in their fatty acid composition, is currently expanding. Such
data are used for physiological, chemotaxonomic and
intrageneric differentiation studies of many organisms such
as bacteria, algae, fungi and vascular plants. Nutritionally,
linoleic and a-linolenic acids are essential for basal metab-
olism in humans, while long-chain polyunsaturated fatty acids
(PUFA) have many beneficial effects on human health
(Pedneault et al., 2006).
Amanita caesarea (Amanitaceae), commonly known as
Caesar’s mushroom, is a highly regarded edible mushroom. It
has a distinctive orange cap, yellow gills and stem. Its value has
been known ever since the time of ancient Romans. Amanita
caesarea is also one of the well-known species used as food in
Turkey. It grows in mixed forests of coniferous and deciduous
Correspondence: Hasan Hu
¨seyin Dog
˘an, Biology Department, Science
Faculty, Selcuk University, Campus, Konya, Turkey. Tel:
þ905358835145. E-mail: hhuseyindogan@yahoo.com
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trees. Although A.caesarea is an important food source in
Turkey, there is no conclusive report available concerning its
antioxidant activity, antimicrobial effects or fatty acid com-
position. The main objectives of this study are (i) to reveal the
antioxidant activity of a methanol extract of A.caesarea, (ii) to
observe the antimicrobial effects of chloroform, acetone and
methanol extracts of A.caesarea against Gram-positive
and Gram-negative bacteria and yeast, and (iii) to characterize
the fatty acid composition of A.caesarea.
Materials and methods
Collection of A.caesarea samples
The samples of A.caesarea were collected in mixed Pinus
brutia,Quercus sp. and Arbutus sp. forest, with elevation of
300 m, on 4 November 2008. The collection site was Karatepe
district, Gazipas¸a, Antalya Province, Turkey, and its
Fungarium number is HD2234.
The species identification was performed by Hasan
Hu
¨seyin Dog
˘an as described in the literature (Galli, 2001).
A stock sample of the species was also deposited at the
Fungarium of the Mushroom Application and Research
Centre, Selcuk University, Konya, Turkey.
Sample preparation
The fruiting bodies of each mushroom sample were dried in a
dehydrator at 37–40 C for 5 d. The dried samples were
homogenized in a household blender at the full speed until
they turned into powder.
Antioxidant activities
Chemicals
b-Carotene, linoleic acid, 2,2-diphenyl-1-picrylhydrazyl
(DPPH), butylated hydroxytoluene (BHT), butylated hydro-
xyanisole (BHA) and a-tocopherol were purchased from
Sigma (Sigma-Aldrich, St Louis, MO). Tween 20, Folin-
Ciocalteu’s phenol reagent (FCR), sodium carbonate and
methanol were purchased from Merck (Darmstad, Germany).
All the chemicals and reagents were of analytical grade and
were obtained from either Sigma or Merck.
Preparation of the methanol extracts for testing antioxidant
activities
Briefly, 100 g of dried and powdered sample was extracted by
stirring in methanol at 60 C for 6 h in a Soxhlet apparatus.
The extract was then filtered through Whatman No. 4 filter
paper and concentrated under vacuum at 45 C using a rotary
evaporator. The extracts were then lyophilized and stored in
the dark at 4 C till further use.
Scavenging effect on DPPH radicals
Methanol extract (1 mL) in a range of concentrations
(0.03–0.5 mg/mL) was added to 1 mL DPPH radical solution
in methanol (the final concentration of DPPH was 0.2 mM).
The mixture was shaken vigorously and kept for 30 min in the
dark, and the absorbance was then measured at 517 nm
against a blank using a Hitachi U-2001 spectrophotometer
(Hitachi High-Tech Co., Kyoto, Japan) (Shimada et al., 1992).
BHT and BHA were employed as standard controls.
Scavenging of DPPH free radicals was calculated in percent-
ages via the following equation:
%Scavenged ¼ðAblank AsampleÞ=Ablank 100
where A
blank
is the absorbance of the control reaction and
A
sample
is the absorbance of the test compound. The extract
concentration providing 50% inhibition (IC
50
) was calculated
from a graph plotting % scavenged against extract concentra-
tion. Tests were performed in triplicate.
b-Carotene–linoleic acid assay
The b-carotene-linoleic acid assay was conducted as
described by Taga et al. (1984). b-Carotene solution (1 mL)
in chloroform (3.34 mg/mL) was pipetted into a flask
containing 40 mg linoleic acid and 400 mg of Tween 20.
The chloroform was then removed by means of a rotary
evaporator at 40 C for 5 min. To the resulting residue,
100 mL of oxygen passed through distilled water was added
slowly, with vigorous agitation to form an emulsion. A 5 mL
aliquot of this emulsion was added to a tube containing
0.2 mL of the 200 mg/mL antioxidant solution, and the
absorbance was measured immediately at 470 nm against a
blank, which consisted of the emulsion without b-carotene.
The tubes were then placed in a water bath at 40 C, and the
absorbance was measured again at 15 min intervals.
Reducing power
Each extract (0.04–0.4 mg/mL) in methanol (2.5 mL) was
mixed with 2.5 mL of 200 mM sodium phosphate buffer (pH
6.6) and 2.5 mL of 1% potassium ferricyanide, and the
mixture was incubated at 50 C for 20 min. Next, 2.5 mL of
10% trichloroacetic acid (w/v) was added, and the mixture
was centrifuged at 200 gfor 10 min. The upper layer (2.5 mL)
was mixed with 2.5 mL of deionized water and 0.5 mL of
0.1% ferric chloride. Finally, the absorbance was measured
at 700 nm against a blank, using a Hitachi U-2001
spectrophotometer.
Determination of the total phenolic content
The total phenolic content of the methanol crude extract was
determined by the Folin–Ciocalteu method with some modi-
fications, according to Singleton and Rossi (1965). The total
phenolic content of the samples was expressed in gallic acid
equivalents, which reflects the phenolic content as the
quantity of gallic acid (mg) contained in 1 g of the sample.
Phenolic composition of A. caesarea
A Shimadzu 1100 series (Shimatzu Co., Kyoto, Japan) high-
performance liquid chromatography (HPLC) equipped with a
SIL-10AD vp autosampler and LC-10Advp pump system, a
diode array detector (DAD) and an Inertsil Agilent Eclipse
XDB column (240 mm 4.60 mm, 5 mm particle size) (Inertsil
Co., Boston, Billerica, MA) was utilized to analyze phenolic
compounds. The mobile phase comprised of (A) 100%
methanol and (B) 3% (v/v) aqueous acetic acid. HPLC
separation was performed as described by Maltas and Yildiz
(2011). Gallic acid, catechin, caffeic acid, p-coumaric acid,
864 H. H. Dog
˘an & G. Akbas¸Pharm Biol, 2013; 51(7): 863–871
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ferulic acid, cinnamic acid and quercetin (Sigma-Aldrich, St
Louis, MO) were used as standards. The samples were run in
triplicate.
Antimicrobial activity
Preparation of the extracts
Chloroform, acetone and methanol were used as solvents.
Each powdered fungus sample (30 g) was suspended with
250 mL of chloroform in a Soxhlet apparatus for 8 h. The
resultant extract was concentrated by means of a rotary
evaporator at 40 C and at low pressure, and the desired phase
was separated from the crude extract with chloroform. Later,
the residue was extracted with acetone and methanol,
respectively. After extraction, all the semi-solid extracts
were dried by a freeze-dryer to yield powders. The powdered
extracts were dissolved in DMSO:PBS (1:1) at a 100 000 mg/
mL concentration and filtered through a sterile filter
(0.45 mm) and stored at 4 C.
Test microorganisms
All the microorganisms were obtained from the Department of
Biology, Faculty of Science, Selc¸uk University. Four Gram-
positive bacteria (Bacillus subtilis ATCC 6633,
Staphylococcus aureus ATCC 6633, Listeria monocytogenes
type 2 NCTC 5348, and Streptococcus pyogenes ATCC 19615)
and five Gram-negative bacteria (Escherichia coli ATCC
35218, Klebsiella pneumoniae ATCC 10031, Pseudomonas
aeruginosa ATCC 15442, Proteus vulgaris ATCC 7829 and
Salmonella enteritidis RSHMB) were chosen as test bacteria.
Candida albicans ATCC 1023 was chosen as a test yeast.
Antimicrobial assay
Brain heart infusion broth (BHIB, Oxoid) was used to
cultivate the bacteria and malt extract broth (MEB, Difco)
was used for the yeast. Each bacterial species obtained
from stock cultures were added into 4–5 mL BHIB and
incubated at 35 C for 24 h. The bacterial cultures were
prepared in the same medium at a density adjusted to 0.5
McFarland turbidity standards (10
8
cfu/mL), and the final
concentration of each bacterial culture was adjusted to 10
5
cfu/mL. The yeast strain obtained from the stock culture was
added into 4–5 mL MEB and incubated at 25 C for 48 h.
After incubation, the final concentration of the yeast was
adjusted to 10
4
cfu/mL.
Determination of antimicrobial activity by microdilution
method
The MIC values were evaluated in accordance with NCCLS
(2008). Amanita caesarea extract in the stock solutions was
prepared at a 20 000 mg/mL concentration in PBS:DMSO
(1:1). MHB (100 mL) was dispensed into each well of a flat-
bottom, 96-well microtiter plate. To prepare serial dilutions,
100 mLofA.caesarea chloroform, acetone or methanol
extract was separately dispensed into MHB-containing
microplate wells (A1, A2, A3, etc.), mixed well and 1/2
dilutions were prepared. Finally, this process was repeated to
generate a dilution series of each extract from 20 000 to
0.305 mg/mL.
After the dilution series of each extract was prepared,
100 mL of each bacterial suspension was added separately into
each well containing the MHB and the mushroom extract
mixture. The current procedure was also repeated for the yeast
in different plate wells.
The absorbance of each well was measured by employing
an ELISA reader at 630 nm (EL 800). After the first
reading was finished, all the plates were covered and
incubated at 37 C for 24 h. Afterwards, the absorbance
was measured again. The first absorbance was subtracted
from the second absorbance, and the difference was used to
calculate the minimum inhibitory concentration (MIC)
values. The lowest concentration that produced an inhibitory
effect was recorded as the MIC for each extract (as described
by Devienne & Raddi, 2002, with some modifications).
Ampicillin (100 mg/mL concentration) for bacteria and
amphotericin B (50 mg/mL concentration) for yeast were
utilized as positive controls. Each experiment was conducted
in triplicate. Due to the lack of correlation and statistical
significance between each bacterial species, statistical ana-
lysis was not performed.
Fatty acid extraction
To obtain the crude oil of the fungus, a powdered fungus
sample (30 g) was suspended with 250 mL of petroleum ether
in a Soxhlet apparatus for 8 h. Oil sample of 0.16–0.20 g was
added to a round-bottom flask containing 4 mL of a 0.5N
methanol NaOH solution. Then, the mixture was boiled in a
water bath for 10 min until saponification occurred. After
saponification, 5 mL of 14% BF
3
–methanol solution was
added to the flask, and the mixture was boiled for 5 min.
Then, the flask was shaken, and 2 mL n-heptane was added.
All the extract mixtures were boiled for 1 min, and 4 mL NaCl
(a saturated solution) was added. Once the extract was
thoroughly mixed, it was transferred into a separating funnel,
and the phases were allowed to separate for 5–10 min. The
lower aqueous phase was discarded, and the upper, light-
yellow-colored phase was aliquoted into phials, which were
stored in a freezer until needed.
Gas chromatography analysis
Gas chromatography analysis was performed by making use
of an HP 6890 model Hewlett Packard Agilent gas
chromatograph with an automatic injector and a flame
ionization detector. A 100 m HP-88 capillary column was
employed in the analysis. The temperature of the injector
block was set to 240 C, and the detector block was set to
250 C.
The column temperature was initially set to 160 Cfor
2 min, and later increased to 185 C at a rate of 4 C per min.
This was followed by a temperature increase by 1 C per min
to 200 C. When the temperature reached 200 C, the column
was held at this temperature for 46.75 min. The analysis was
completed in 70 min. The helium flow was set to 1 mL/min.
Alltech and Accu standards were applied for identification of
the fatty acid content. The results were rendered as
percentage of the total fatty acids. The standard errors
ranged from 1 to 3%, and three GC analysis results were
evaluated together.
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Results and discussions
Antioxidant activity results
The scavenging effect on DPPH radicals
The DPPH radical scavenging effects of A.caesarea methanol
extract, along with those of the BHA and BHT controls
increased with increasing the concentration from 0.03 to
0.5 mg/mL (Figure 1). The scavenging values recorded at
0.03 mg/mL concentration are 0.049 mg/mL for A.caesarea,
0.045 mg/mL for BHT and 0.056 mg/mL for BHA, while the
scavenging values at 0.5 mg/mL are 0.039 mg/mL for
A.caesarea, 0.031 mg/mL for BHT and 0.026 mg/mL for
BHA. As illustrated in Figure 1, the scavenging effect of
A.caesarea extract on DPPH radicals increased with
increasing concentrations.
The IC
50
value of A.caesarea extract is higher than BHA
and BHT. The IC
50
values were 0.7615 mg/mL for
A.caesarea, 0.35519 mg/mL for BHA and 0.4119 mg/mL
for BHT (Figure 2). A lower IC
50
value indicates a higher
antioxidant activity (Pourmorad et al., 2006). The inhibition
values of A.caesarea extract and the standards on the DPPH
radicals at a concentration of 0.5 mg/mL were 40.91% for
A.caesarea, 60.60% for BHA and 53% for BHT.
In previous studies, the scavenging effects of the mush-
room extracts ranged from 36% to 96% at a concentration of
5–10 mg/mL. In view of the fact that different methods and
concentrations have been used in the literature, there are no
standard levels for measurement of scavenging effects. Some
studies can be summarized as follows. Yang et al. (2002)
studied a number of commercially important mushrooms
[Flammulina velutipes (Curtis) Singer (Physalacriaceae),
Lentinula edodes (Berk.) Pegler (Marasmiaceae), Pleurotus
ostreatus (Jacq.) P. Kumm. and P. cystidiosus O.K.Mill.
(Pleurotaceae)], and they established that the scavenging
effects of methanol extracts of the said mushrooms varied
between 42.9% and 81.8% at 6.4 mg/mL concentration. The
scavenging effect of a methanol extract from Volvariella
volvacea (Bull.) Singer (Pluteaceae) was found 57.8% at
9 mg/mL concentration (Cheung et al., 2003). Mau et al.
(2004) applied a 10 mg/mL concentration for their studies,
which reported scavenging effects of 78.8, 79.9 and 94.1% for
Termitomyces albuminosus (Berk.) R.Heim (Agaricaceae),
Grifola frondosa (Dicks.) Gray (Meripilaceae) and Morchella
esculenta (L.) Pers. (Morchellaceae), respectively.
Additionally, Lee et al. (2008) studied the fruiting body and
mycelia of Hypsizygus marmoreus (Peck) H.E.Bigelow
(Lyophyllaceae) with hot water and methanol extraction.
According to their results, the scavenging effects of the
fruiting body and mycelia ethanol extracts, at a concentration
of 5 mg/mL, were both 75.5%, while the scavenging effects of
Figure 1. DPPH radical scavenging effects of
A.caesarea, BHA and BHT.
Figure 2. IC
50
values of A.caesarea, BHA
and BHT.
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the fruiting body and mycelia hot water extracts were 36.8
and 55.5%, respectively, also at 5 mg/mL concentration. At
10 mg/mL concentration, the scavenging effect of Russula
delica Fr. (Russulaceae) extract was 26% (Yaltirak et al.,
2009). Compared with the inhibition values reported in the
aforementioned studies, A.caesarea extract was effective at a
much lower concentration. In the present study, inhibition
levels by the A.caesarea extract reached 40.91% at 0.5 mg/
mL concentration, while those of the BHA and BHT controls
were 60.6% and 53%, respectively.
b-Carotene–linoleic acid assay
The rate of absorbance change was calculated from T
0
to
120th min and used to calculate the coefficient of oxidation
prevention as a percent (%). The bottom absorbance curve
was employed as a control sample. Antioxidant activity was
assayed as an ability to inhibit the peroxidation of linoleic
acid. The inhibition values of A.caesarea extract were
determined to be higher than those of Trolox, but similar to
BHT and lower than BHA. Amanita caesarea extract, BHA,
BHT and Trolox exhibited 71.29, 85.14, 74.12 and 50.51%
inhibition, respectively (Figure 3).
According to the literature, inhibition values of mushroom
extracts vary between 50% and 96% at different concentra-
tions. The antioxidant activity of methanol extracts of young
and mature Agaricus brasiliensis Fr. (Agaricaceae) specimens
were evaluated with the b-carotene–linoleic assay, and they
were found to inhibit oxidation with 92% at 0.2 mg/mL
concentration (Soares et al., 2009). Gu
¨rsoy et al. (2009)
studied six Morchella species (Morchella rotunda (Fr.) Boud.,
M.esculenta (L.) Pers. var. umbrina (Boud.) S. Imai, M.
deliciosa Fr., M.elata Fr., M.conica Pers. and M.angusticeps
Peck.), and they ascertained that M.esculenta var. umbrina
and M.angusticeps were the most active species with 96.89%
and 96.88%, respectively, at 4.5 mg/mL concentration.
Sariku
¨rkcu
¨et al. (2010) observed A.caesarea,Clitocybe
geotropa (Bull.) Que
´l. (Tricholomataceae) and Leucoagaricus
pudicus (Bull.) Bon, and they discovered that L. pudicus
possessed the highest oxidation level with 81.8%, followed by
A. caesarea with 70.1% and by C. geotropa with 61.3% at
25.5 mg/mL concentration. According to the proposed previ-
ous study, A.caesarea has a high oxidation level (71.29%)
even at a low concentration (2.284 mg/mL).
Reducing power
The reducing power of A.caesarea extract demonstrated a
parallelism with its increased concentration (Figure 4).
Namely, a higher absorbance indicates a higher reducing
power. The highest reducing power was observed with BHA
(2.021), followed by BHT (1.869) and A.caesarea (0.36) at
0.075–1.2 mg/mL concentration.
Figure 4. Reducing power of A.caesarea and
synthetic antioxidants.
Figure 3. b-Carotene–linoleic acid assay.
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Yang et al. (2002) observed that the reducing power of
mushrooms in their study exceeded 1.28 at 40 mg/mL
concentration, with the reducing power of each species
ordered from the highest to the lowest, as follows: Pleurotus
ostreatus ¼P. cystidiosus4Lentinula edodes4F. velutipes.
According to Elmastas¸ et al. (2007), the reducing power of R.
delica and Verpa conica (O.F. Mu
¨ll.) Sw. (Morchellaceae)
extracts were 1.32 and 1.22, respectively, at 200 mg/mL
concentration. At 20 mg/mL concentration, the reducing
powers of A.caesarea,C.geotropa and L.pudicus were
1.5, 1.2 and 1.3 mg/mL, respectively (Sariku
¨rkcu
¨et al., 2010).
In the current study, the reducing power of A.caesarea was
0.451 at 1.2 mg/mL concentration. In comparison with the
previous studies described above, A.caesarea possessed a
high reducing power at a low concentration.
Total phenolic content
The total phenolic content of the samples is expressed as
milligram of gallic acid per gram equivalent of dry mush-
room. The amount of phenolic compounds in the methanol
extract of A. caesarea was determined to be 0.642 mg/g gallic
acid equivalents. A number of common edible mushrooms,
which are widely consumed in Asian cultures, have been
found to possess antioxidant activities that are well correlated
with their total phenolic content (Cheung et al., 2003).
Phenolic compounds of A. caesarea
Some selected phenolic acids and flavonoids of the extract
were separated and compared with authentic standards by
means of reverse-phase HPLC for identification. The phenolic
composition of A.caesarea has been reported here for the
first time (Table 1).
Seven components of the methanol extract of A.caesarea
were analyzed, and four components were identified: cat-
echin, p-coumaric acid, ferulic acid and cinnamic acid. There
were substantial qualitative and quantitative differences in the
components of the extracts. Catechin was the predominant
phenolic compound with a value of 32.5 mg/g, followed by
ferulic acid with 7 mg/g, p-coumaric acid with 6 mg/g, and
cinnamic acid with 4.6 mg/g. Nonetheless, the extract did not
contain any flavonoids, such as quercetin, caffeic acid and
gallic acid.
Antioxidant, antimicrobial, anti-allergy and anticancer
effects of catechin have been reported in a number of earlier
studies (Kondo et al., 2000; Shimamura et al., 2007). Catechin
was found in R.delica with 5.33 mg/g by Yaltirak et al.
(2009). In the present study, it was found in high concentra-
tion (32.5 mg/g). The high antimicrobial activity shown by
A.caesarea may be due to the presence of catechin.
Ferulic acid, like many other phenols, is an antioxidant
in vitro in the sense that it is reactive toward free radicals,
such as reactive oxygen species (ROS). ROS and free radicals
are implicated in DNA damage, cancer and accelerated cell
aging. Ferulic acid may also have a direct antitumor activity
against breast cancer and liver cancer, and it may have pro-
apoptotic effects in cancer cells, thereby leading to their
destruction. Ferulic acid may be effective in preventing
cancer induced by exposure to carcinogenic compounds
(Kampa et al., 2004).
Coumarin derivatives are substances important for human
health. They have anti-thrombotic, anti-inflammatory and
vasodilatory effects, coupled by antiviral and antimicrobial
activities. Coumarin was also found to inhibit C. albicans
in vitro. As a group, coumarins have been found to stimulate
macrophages, which could have an indirect negative effect on
infections. ‘‘More specifically, coumarin has been used to
prevent recurrences of cold sores caused by HSV-1 in
humans’’ (Cowan, 1999).
Cinnamic acids are common representatives of a wide
group of phenylpropane-derived compounds that are in the
highest oxidation state. Cinnamic acids are effective against
viruses, bacteria and fungi (Cowan, 1999).
Antimicrobial results
According to Craig (1998), in order to evaluate antimicrobial
activity, MIC values ought to be measured from the 4th
through the 16th dilutions. The antimicrobial effects of A.
caesarea against bacteria and yeast were measured in
compliance with the following ranges (Gu
¨lay, 2002;
Morales et al., 2008):
1-MIC values are lower than 100 mg/mL ¼antimicrobial
activity is high.
2-MIC values are between 100 mg/mL and 500 mg/mL ¼
antimicrobial activity is moderate.
3-MIC values are between 500 mg/mL and 1000 mg/mL ¼
antimicrobial activity is weak.
4-MIC values are more than 1000 mg/mL ¼no antimicrobial
effect.
Pursuant to the quoted ranges, the antimicrobial results are
provided in Table 2. Amanita caesarea exhibited different
antimicrobial effects in various concentrations against each
test microorganism. The maximum inhibitory effect on the
test microorganisms was observed with an acetone extract
(MIC value, 4.8 mg/mL in the 13th dilution) against
Table 2. MIC values of A. caesarea extracts (mg/mL)
a
.
Microorganisms Chloroform Acetone Methanol
B. subtilis 39 39 39
S. aureus 39 39 39
L. monocytogenes 39 78 39
S. pyogenes 39 78 78
C. albicans 39 4.8 39
E. coli 39 312.5 156
K. pneumoniae 312.5 39 39
P. aeruginosa 39 39 39
P. vulgaris 39 39 39
S. enteritidis 39 39 39
a
5100 mg/mL ¼High, 100–500 mg/mL ¼Moderate and 500–1000 mg/
mL ¼Low.
Table 1. Phenolic compounds of A. caesarea.
Phenolic compounds Composition (mg/g)
1. Caffeic acid ND
2. Catechin 32.5
3. Cinnamic acid 4.6
4. Ferulic acid 7
5. Gallic acid ND
6. p-Coumaric acid 6
7. Quercetin ND
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C. albicans. Overall, the methanol extract was observed to
display the maximum antimicrobial effect with values gen-
erally lower than 100 mg/mL, placing it in the high-activity
category. The microorganisms inhibited at this level were
B.subtilis,S.aureus,L.monocytogenes,C.albicans,
K.pneumoniae,P.aeruginosa,P.vulgaris and S.enteritidis
(MIC values, 39 mg/mL in the 9th dilution). The effects of the
methanol extract against S. pyogenes and E.coli were highly
and moderately active (MIC values, 78 and 156 mg/mL in the
6th and 7th dilutions, respectively). The MIC values of
chloroform and acetone extracts were almost identical with
the MIC values of 39 mg/mL. The lowest antimicrobial effect
was noted in the chloroform extract against K.pneumoniae
and acetone extract against E.coli (MIC values, 312.5 mg/mL
in the 6th dilution).
In general, methanol and acetone extracts of A.caesarea
were more effective than chloroform extracts against bacteria
and yeast. The most effective MIC concentrations of the
extracts were typically measured between the 6th and 9th
dilutions (MIC values, 312.5–39 mg/mL), and these results
demonstrated that the inhibition values were lower than
100 mg/mL or between 500 and 1000 mg/mL.
The current results were verified by previous studies.
According to Yoon et al. (1994), G.lucidum had a good
antimicrobial effect against Proteus vulgaris (MIC, 1.25 mg/
mL) and Escherichia coli (MIC, 1.75 mg/mL), and six species
of bacteria had MIC values larger than 5 mg/mL. Within the
study, MIC values were generally measured between 78 and
312.5 mg/mL, and the present results are better than those of
Yoon et al. (1994). Gbolagade et al. (2007) studied the
antimicrobial effects of certain fungal species by the
employment of micro dilution methods, and they established
that the MIC concentration of Marasmius jodocodo Henn.
(Marasmiaceae) was 2.75 mg/mL against E. coli, while T.
robustus was 15.75 mg/mL against M. bourlardii. Janes
ˇet al.
(2007) applied the broth micro dilution test for screening of
antibacterial activity on the extracts of higher and endophytic
fungi. Among the tested extracts, three significant antibac-
terial activities were identified from the extracts of Amanita
virosa Secr. (Amanitaceae) and Cortinarius praestans
(Cordier) Gillet (Cortinariaceae) against P.aeruginosa and
Staphylococcus aureus, respectively, and the extract of
endophytic fungus Truncatella hartigii (Tubeuf) Steyaert
(Amphisphaeriaceae) against Enterococcus faecalis and
S.aureus. Quereshi et al. (2010) tested the antimicrobial
activity of various solvent extracts of G.lucidum (40 mg/mL
concentration) against six species of bacteria. Acetone extract
showed the maximum antibacterial activity, whereas the most
susceptible bacterium recorded was Klebsiella pneumoniae.
Bala et al. (2011) investigated the antimicrobial effect of 47
different specimens from Australia, and they ascertained that
water and ethanol extracts were more effective against
S. aureus than E. coli, whereas an inconsiderable number of
hexane extracts showed better results for their potential
antimicrobial effect against E. coli at higher concentration. In
general, a number of macrofungi from the genera Agaricus,
Amanita,Boletus,Cantharellus,Fomitopsis,Hohenbuehelia,
Lentinus,Ramaria and Strobilomyces demonstrated good
inhibition rates. Aqueous and methanol extracts of Trametes
hirsuta (Wulfen) Lloyd (Polyporaceae) were tested against
pathogenic fungi and bacteria. Maximum antibacterial activ-
ity of the aqueous extract of T.hirsuta was found against
S.aureus compared to that of the methanol extract.
Significant antifungal activity of the aqueous extract was
found against Aspergillus flavus compared to that of the
methanol extract (Sivaprakasam et al., 2011). The antibac-
terial effects of the extract from three mushrooms G.lucidum,
Auricularia auricula (L.) Underw. (Auriculariaceae) and
Pleurotus floridanus Singer (Pleurotaceae) were studied
against S.aureus and E.coli.Auricularia auricula displayed
significant antibacterial activity against S.aureus. P. flor-
idanus showed some antibacterial activity, while G. lucidum
did not demonstrate any antibacterial activity. None of the
extracts exhibited any activity against E.coli (Iftekhar et al.,
2011).Antimicrobial activity of Ganoderma praelongum
Murrill, G.resinaceum Boud. and G.lucidum were evaluated
against 30 strains of clinical isolates of methicillin resistant
and methicillin sensitive S.aureus. The maximum activity of
crude extracts was exhibited by ethyl acetate. The MIC
of sesquiterpenoid extracts of G.praelongum was
Table 3. Percentage of fatty acids of A. caesarea.
Carbon
numbers A. caesarea
Common and
systematic names
C 6:0 0.01 0.01 Caproic acid
C 8:0 0.01 0.01 Caprylic acid
C 10:0 0.02 0.01 Capric acid
C 11:0 0.03 0.01 Undecylic acid
C 12:0 0.03 0.01 Lauric acid
C 13:0 0.01 0.01 Tridecylic acid
C 14:0 0.17 0.01 Myristic acid
C 15:0 0.19 0.01 Pentadecylic acid
C 16:0 15 0.04 Palmitic acid
C 17:0 0.04 0.01 Margaric acid
C 18:0 6.09 0.01 Stearic acid
C 20:0 0.07 0.04 Eicosanoic acid
C 21:0 0.20 0.01 Heneicosanoic acid
C 22:0 0.01 0.01 Docosanoic acid
C 24:0 0.01 0.01 Tetracosanoic acid
PSFA* 21.46 0.01
C 14:1n5 0.03 0.01 Myristoleic acid
C 15:1n5 0.01 0.01 Pentadecenoic acid
C 16:1n7 0.63 0.01 Palmitoleic acid
C 17:1n8 0.13 0.01 9-Heptadecanoic acid
C 18:1n9 58 0.06 Oleic acid
C 20:1n9 0.20 0.04 11-Eicosenoic acid
C 22:1n9 0.01 0.01 13-Docosanoic acid
C 24:1n9 0.01 0.01 15-Tetracosenoic acid
PMUFA 59.07 0.02
C 18:2n6 19.02 0.02 Linoleic acid
C 18:3n6 0.06 0.01 6-9-12 Octadecatrienoic acid
C 18:3n3 0.03 0.01 Linolenic acid
C 20:2n6 0.01 0.01 11,14-Eicosadienoic acid
C 20:3n6 0.01 0.01 8,11,14-Eicosatrieonic acid
C 20:3n3 0.01 0.01 Eicosatrienoic acid
C 20:4n6 0.12 0.01 5-8-11-14 Eicosatetraeonic acid
C 20:5n3 0.10 0.01 5-8-11-14-17 Eicosapentaenoic acid
C 22:2n6 0.05 0.01 cis-13,16-Docosadienoic acid
C 22:3n3 0.01 0.01 13-16-19 Docosatrienoic acid
C 22:4n6 0.03 0.01 7-10-13-16 Docosatetraenoic acid
C 22:5n6 0.01 0.01 4-7-10-13-16 Docosapentaenoic acid
C 22:5n3 0.01 0.01 7-10-13-16-19 Docosapentaenoic acid
C 22:6n3 0.03 0.01 4-7-10-13-16-19 Docosahexaenoic acid
PPUFA
a
19.48 0.03
a
SFA: saturated fatty acid, MUFA: mono unsaturated fatty acid, PUFA:
polyunsaturated fatty acid.
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0.390–6.25 mg/mL. Diterpenoids and triterpenoids displayed
a moderate activity, while polysaccharides IIIa and IIIb
showed a weak activity. All bacterial strains were resistant to
polysaccharides I and II (Ameri et al., 2011).
The current results are similar or more effective than those
reported in the literature. To the best of our knowledge, there
have previously been no reports on the antimicrobial effects
of A.caesarea, and these results have been reported here for
the first time.
Fatty acids
Saturated fatty acids (SFA), monounsaturated fatty acids
(MUFA) and polyunsaturated fatty acids (PUFA) of
A.caesarea were analyzed by gas chromatography
(Table 3). A total of 37 fatty acids were established. These
fatty acids varied in the length from C6 to C24. The largest
component of the total fatty acid was identified as C18:1 !9
(oleic acid). In addition, MUFA, measured as 59.07% of the
total fatty acid composition, were more abundant than SFA
(21.46%) and PUFA (19.48%).
The most abundant fatty acid recorded in A.caesarea was
oleic acid (58.6%), followed by linoleic acid (19.02%),
palmitic acid (14.59%) and stearic acid (6.09%). The said
four most abundant fatty acids constituted 97.76% of the total
fatty acid pool.
The main fatty acid components of Lactarius deliciosus (L.)
Gray (Russulaceae), Sarcodon imbricatus (L.) P.
Karst.(Bankeraceae) and Tricholoma portentosum (Fr.) Que
´l.
(Tricholomataceae) consisted of MUFA, while PUFA were the
most abundant components of Agaricus arvensis Schaeff.
(Agaricaceae) and Leucopaxillus giganteus (Sowerby) Singer
(Tricholomataceae) (Barros et al., 2007). Unsaturated fatty
acids were found at higher concentrations than saturated fatty
acids in the total fatty acids of the mushrooms analyzed by
Mauger et al. (2003). In the present study, the high MUFA
content of A.caesarea (59.07%) is consistent with these results.
Palmitic acid is the most common saturated fatty acid in
plants and animals. This is the primary fatty acid from which
other longer fatty acids are synthesized. Palmitic acid is not
found in a free form in nature like other fatty acids and the
level of palmitic acid in A.caesarea is relatively high (15%).
The most common MUFA is oleic acid. This acid is
utilized in soap-making, wax production, medicine, and
textile and leather industries. Oleic acid may hinder the
progression of adrenoleukodystrophy, a fatal disease that
affects the brain and adrenal glands. Oleic acid may be
responsible for the hypertensive (blood pressure-reducing)
effects of olive oil. Adverse effects have also been docu-
mented; however, both oleic and monounsaturated fatty acid
levels in the membranes of red blood cells have been
associated with an increased risk of breast cancer. The oleic
acid content in A.caesarea was measured as 58%, a useful
level for dietary purposes. In the current study, trans fatty acid
isomers were not found.
The fatty acid composition of Agaricus bisporus (J.E.
Lange) Imbach, A.campestris L., Coprinus comatus (O.F.
Mu
¨ll.) Pers. (Agaricaceae), Boletus edulis Bull. (Boletaceae),
P.ostreatus,Oudemansiella radicata (Relhan) Singer and
Armilleria mellea (Vahl) P. Kumm. (Physalacriaceae) was
studied, and the amount of unsaturated fatty acids present was
higher than that of saturated fatty acids. Linoleic acid was
determined to be common in all mushroom species. In
addition, palmitic acid, oleic acid, stearic acid and arachidic
acid were the most abundant fatty acids identified in a study
of various fungi (Yilmaz et al., 2006). Oleic acid and linoleic
fatty acids of A. caesarea were the most abundant fatty acids.
Palmitic and stearic acid were the next most predominant
components of A.caesarea. Linoleic acid, an essential fatty
acid, comprised 19.02% of A.caesarea in the total fatty acids.
Conclusions
The antioxidant and antimicrobial effects of A.caesarea were
measured, and its unsaturated fatty acid composition was
revealed to be relatively high. Fungal species can be a source
of healthy food, contributing high levels of antioxidants,
antimicrobial effects and unsaturated fatty acids.
The present results indicate that economically important
and edible mushrooms demonstrate significant antioxidant
and antimicrobial features, and they are a good source of fatty
acids. Therefore, these studies should be expanded to other
economically important and edible mushrooms.
Declaration of interest
The authors are indebted to the Foundation TUB_
ITAK
(TBAG/109T584) and the Scientific Research Projects
(BAP) Coordinating Office (BAP/09201151) at Selc¸uk
University for their financial support of the current work.
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... Especially, in vitro studies showed that some Amanita mushrooms such as A. augusta and A. muscaria exhibited potentially anti-inflammatory activity [4,5]. A. caesarea possesses antioxidant and antimicrobial [6,7,8], lowering cholesterol [9], and neuroprotective activities [10][11][12]. Previous studies showed that this mushroom presented phenolics [7,8,[13][14][15][16], sterols [17], alkaloids [9,18], polysaccharides [11,19,20], and fatty acids [7,21]. ...
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... [48,49] Catechin is a type of phenolic compound present in many foods, plants, fruits, particularly most abundant in green tea, red wine, chocolate, cocoa, etc. Various pharmacological activities of catechin include antioxidant, antimicrobial, anti-cancer, anti-allergy, anti-diabetic activities. [50] Benzoquinone derivatives naturally occurring in most of the living organisms, play important roles such as electron transfer and oxidative phosphorylation. Antimicrobial, antitumor, anticoagulant, antimalarial, antioxidant, antifungal, anti-inflammatory properties of benzoquinone derivatives have been reported. ...
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Present study aimed to establish the stimulatory effects of bee drone larvae (BDL) on the androgenic effects and growth performance of goat male kids (GMK). The effects of BDL on growth and testosterone hormone levels were investigated in Saanen male kids. A total of 26 Saanen male kids (13 heads control, 13 heads treatment groups) were used for determining the effects of BDL 60 days after the weaning period. BDL was obtained from "good beekeeping practices" hives. Hormone levels, growth trials, testes characteristics, and body measurements were determined every 14 days on the days 75, 90, 105, 120, and 135 of the trial. The increasing level of testosterone hormone in the treatment group on 135 days strengthened the hypothesis that the BDL could have greater effects in case of more application that is expensive and considering the time of maturity of Saanen GMK. The lipid composition of BDL was identified by GC‐MS. Oleic acid (64.75%) and palmitic acid (26.08%) were the dominant lipid compounds of BDL. Additionally, the phenolic/organic acid profile investigated by HPLC‐DAD revealed that trans ‐aconitic acid (11.20±0.32 μg/g) and fumaric acid (5.03±0.41 μg/g) were found as major compounds in BDL.
... Thus they constitute the essential lipids or fatty acids that must be obtained through the diet [31]. Amanita caesaria is an important mushroom found in Turkey, with thirty-seven (37) different fatty acids in its sporocarp [32]. In Nigeria and Ethiopia, P. ostreatus was rich in linoleic acid up to 27.6 and 61.1%, respectively [33,34]. ...
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Mushrooms are macroscopic fungi consumed for their rich nutritious taste, aroma and health benefits. Mushrooms grow naturally in the wild as saprophytes and are available in most African countries in the rainy season. Mushrooms have long been recognised as functional foods and nutraceuticals due to the many health benefits attributable to their richness in bioactive components. Some health benefits include anticancer, hepatoprotective, anti-viral, cholesterol-lowering, immune boosting , antioxidant and anti-ageing properties. Despite these established uses, many mushrooms have not been popularly domesticated in Nigeria, thereby hindering the functional use of this nature's gem as promising nutraceuticals. Besides, the mycophobic attitudes of many citizens have significantly prevented their exploitation. This review showcases mushrooms as affordable and exotic functional foods, rich in phyto-chemicals with great benefits for wellness. This suggests that a further boost in knowledge is required for the populace to embrace mushrooms' cultivation, consumption, and medicinal applications .
... The bioactivity, chemical composition, as well as AOA and NPE of edible mushroom Amanita caesarea (Caesar's mushroom) have been reported (Doğan and Akbaş 2013;Li et al. 2017). The AE of A. caesarea improve cell viability, restored mitochondrial function, inhibited the overproduction of intracellular ROS and Ca 2+ , and suppressed the high expression levels of cleaved-caspase-3 and calpain 1 enzymes, apoptosis-inducing factor (AIF) in the AD-mouse model, as well as alleviated the deposition of Aβ in the brain. ...
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Diversity of wild and cultivated macrofungi as edible and medicinal mushrooms has long been known by humans as a source of valuable food and medicines used by tradipraticians. In the fungal kingdom, macrofungi taxonomically belong to two phyla, the Basidiomycota (class Agaricomycetes) and Ascomycota (class Pezizomycetes). Macrofungi have been used in traditional Asian and European Medicines, and based on 90,000 known worldwide distributed mushroom species, are considered an important resource for modern clinical and pharmacological research. They are regarded as a source of high- and low-molecular-weight bioactive compounds (alkaloids, lipids, phenolics, polysaccharides, proteins, steroids, terpenoids, etc.) with more than 130 therapeutic effects (anti-inflammatory, antimicrobial, antioxidant, antitumor, antiviral, cytotoxic, hepatoprotective, hypocholesterolemic, hypoglycemic, hypotensive, immunomodulatory, etc.). There is also scientific evidence of using macrofungi as neuroprotectants, that is, Agaricus blazei (= Agaricus subrufescens), Ganoderma lucidum, Grifola frondosa, Hericium erinaceus, Pleurotus ostreatus, and Trametes versicolor. However, their neuroprotective effects have not been fully explored. This review discusses recent advances in research on the neuroprotective potential of macrofungi and perspectives for their application as neuroprotectants in biomedicine to prevent, support, or cure neurodegenerative disorders.
... The bioactivity, chemical composition, as well as AOA and NPE of edible mushroom Amanita caesarea (Caesar's mushroom) have been reported (Doğan and Akbaş 2013;Li et al. 2017). The AE of A. caesarea improve cell viability, restored mitochondrial function, inhibited the overproduction of intracellular ROS and Ca 2+ , and suppressed the high expression levels of cleaved-caspase-3 and calpain 1 enzymes, apoptosis-inducing factor (AIF) in the AD-mouse model, as well as alleviated the deposition of Aβ in the brain. ...
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Badalyan S.M. et Rapior S. The neurotrophic and neuroprotective potential of macrofungi. In: Medicinal Herbs and Fungi – Neurotoxicity vs. Neuroprotection. Agrawal D.C. et Dhanasekaran M. (Eds). Publisher Springer. Chapter 2: 37-78 (2021). doi:10.1007/978-981-33-4141-8_2 ____ Diversity of wild and cultivated macrofungi as edible and medicinal mushrooms has long been known by humans as a source of valuable food and medicines used by tradipraticians. In the fungal kingdom, macrofungi taxonomically belong to two phyla, the Basidiomycota (class Agaricomycetes) and Ascomycota (class Pezizomycetes). Macrofungi have been used in traditional Asian and European Medicines, and based on 90,000 known worldwide distributed mushroom species, are considered an important resource for modern clinical and pharmacological research. They are regarded as a source of high- and low-molecular-weight bioactive compounds (alkaloids, lipids, phenolics, polysaccharides, proteins, steroids, terpenoids, etc.) with more than 130 therapeutic effects (anti-inflammatory, antimicrobial, antioxidant, antitumor, antiviral, cytotoxic, hepatoprotective, hypocholesterolemic, hypoglycemic, hypotensive, immunomodulatory, etc.). There is also scientific evidence of using macrofungi as neuroprotectants, that is, Agaricus blazei (= Agaricus subrufescens), Ganoderma lucidum, Grifola frondosa, Hericium erinaceus, Pleurotus ostreatus, and Trametes versicolor. However, their neuroprotective effects have not been fully explored. This review discusses recent advances in research on the neuroprotective potential of macrofungi and perspectives for their application as neuroprotectants in biomedicine to prevent, support, or cure neurodegenerative disorders. Corresponding authors: s.badalyan@ysu.am, sylvie.rapior@umontpellier.fr
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