Mushroom as the Potential Source of New Generation of Antioxidant:

A Review

 

Somanjana Khatua, Snigdha Paul, Krishnendu Acharya*

Molecular and Applied Mycology and Plant Pathology Laboratory, Department of Botany,

University of Calcutta, West Bengal, India.

*Corresponding Author E-mail: krish_paper@yahoo.com

 

Reactive oxygen species (ROS) are induced by various endogenous and exogenous sources. Although almost all organisms are equipped with antioxidant defence systems, which are often inadequate to completely prevent oxidation stress-induced damage. Therefore, antioxidant supplements or natural products containing antioxidants may be used to reduce oxidative damage to the human body. Mushrooms have been part of the normal human diet for thousands of years and in recent times, the amounts consumed have risen greatly involving a large number of species. The main bioactive components of mushroom are phenolic compounds (phenolic acid and flavonoids), tocopherols, ascorbic acid, carotenoids. Polysaccharides are also important biologically active ingredients. The higher antioxidant activity is reflected by lower EC₅₀ value. Austreus hygrometricus, Fistulina hepatica, Phellinus linteus, Pleorotus squarrosulus, Polyporus grammocephalus, Macrocybe gigantea show higher antioxidant potential. This review will discuss about ROS, their harmful effect on biological systems and antioxidant property as well as comparative antioxidant activity of mushrooms with special attention on some popular edible and medicinal ones.

 

 

 

INTRODUCTION:

The reasons behind oxygen toxicity were vague until 1954 when Gershman published his free radical theory of oxygen toxicity¹. Then in 1956, Harman proposed relation of free radicals in the ageing process². The last two decades have been very important to the antioxidant research. Around the world a special attention has been executed in studying the natural antioxidants in foods³.

 

Almost all organisms are well protected against free radical damage. When the mechanism of this antioxidant defence system becomes unbalanced, deterioration of physiological functions may occur⁴. Hence, there is currently great interest in using dietary supplements containing antioxidants. The most commonly used synthetic antioxidants at the present time are butylated hydroxyanisole (BHA), butylhydroxytoluene (BHT), propyl gallate and tert-butylhydroxyquinone. However, BHA and BHT have restricted use in foods as they are suspected to be carcinogenic and to cause liver damage⁵. Therefore, there is growing interest in the use of natural additives as potential antioxidants.

 

This may explain why there is currently much research on the application of antioxidants from natural products.

 

Mushrooms have been part of the normal human diet for thousands of years and in recent times, the amounts consumed have risen greatly involving a large number of species. Mushrooms are valuable health foods since they are low in calories, fats, and minerals⁶. This review examines the available evidences for the role of mushroom as antioxidant. A discussion is also dedicated to free radicals especially reactive oxygen species (ROS) and their effect on biological systems.

 

FREE RADICALS AND THEIR SOURCES:

Free radicals can be defined as molecules or molecular fragments containing one or more unpaired electrons in atomic or molecular orbitals⁷. They are generally unstable and attack quickly the nearest stable molecule to capture the needed electron for gaining stability. Major sources of free radicals are presented in figure 1. Free radicals derived from molecular oxygen are usually known as ROS and represent the most important class of radical species generated in living systems⁸. The term ROS includes not only free radicals (superoxide radical, hydroxyl radical) but also molecules such as hydrogen peroxide, singlet oxygen and ozone⁹. Superoxide anion is considered as the primary ROS as it forms by addition of one electron to molecular oxygen. The less reactive superoxide radical can interact with other molecules through enzyme or metal catalysed processes generating secondary ROS such as hydrogen peroxide and hydroxyl radical^{8, 10}. Table 1 summarizes different types of free radicals with their mode of generation.

 

OXIDATIVE STRESS:

Overproduction of ROS results in oxidative stress. When generation of these species exceeds the system`s ability to neutralise and eliminate them, such stresses occur. At high concentration, ROS can damage cell structure, nucleic acid, lipids and proteins^8,17. Mitochondrial lipid membrane is easily attacked by ROS as mitochondria are the most important source of ROS. This attack resulted lipid peroxidation. Lipid peroxidation results in highly reactive lipid radical (L^.) and eventually forms peroxyl radical (LOO^.). Peroxyl radical reacts with other adjacent lipids producing hydroperxides lipids (LOOH) that easily decomposes to form new lipid radical⁸. Other products of peroxidation process are malondialdehyde (MDA) and      4-hydroxy-2-nonenal (HNE). Both are mutagenic. The intracellular damage causes Bcl-2 to activate Bax. Bax creates holes in the outer mitochondrial membrane and cytochrome C releases to cytosol. It signals for programmed cell death (apoptosis) and cell is destroyed¹⁸.

 

ROS induced DNA damage involves single or double stranded DNA breaks, purine, pyrimidine or deoxyribose modifications and DNA cross-links. Hydroxyl radical can cause DNA lesion by formation of 8-OH-G, a potential biomarker of carcinogensis¹⁹. MDA, product of lipid peroxidation, can react with DNA bases G, A and C to form adducts M₁G, M₁A and M₁C respectively. It is confirmed that M₁G can cause transversions to T and transitions to A and thus is mutagenic. Permanent modification of DNA may results in mutagenesis, carcinogenesis and ageing²⁰. ROS can oxidize the side chains of all amino acids particularly cysteine and methionine residues in protein. There are a number of highly sensitive methods to measure the concentration of protein-carbonyl group which are generated by ROS-mediated protein oxidation¹⁰.

 

 

 

Sources                                                      Occurs through

	Endogenous sources Nutrient metabolism Ageing process Inflammation		Homolytic fission  of covalent bond (requires high energy from high temperature, UV/ ionizing radiation)

 

 

                                                                                                          

                                                                                                                                                                                          

Free radical

                                                      

Loss of single electron from normal molecule

                                                    

Exogenous sources Drugs Tobacco smoke Ionizing, UV radiation Air pollution Organic solvents Pesticide Extreme exercise

                                                                                                                                                                    

 

 

	Addition of single electron to normal molecule

 

 

 

 

 

 

Figure 1: Major sources of free radical and chemistry behind the generation of free radical ^{9, 11}

 

Table 1: Reactive oxygen species of biological interest

Sub classes of reactive species	Generation	Remarks	Ref
Superoxide (O2.-)	By products in electron transfer chain of chloroplast, mitochondria (from both complex I and III), plasma membrane; NADPH oxidaeses, xanthine oxidase. O2+e-  →  O2.-	It is strongly charged to readily cross the inner mitochondrial membrane and release into matrix.	9, 12
Hydroxyl radical (.OH)	Fenton`s reaction H2O2+O2+Fe2+ → .OH+OH-+Fe3+ Haber-Weiss reaction O2.-+H2O2 → .OH+OH-+O2	Half life of ~10-9s, most toxic among all ROS, reacts immediately after formation.	11, 13
Hydrogen peroxide (H2O2)	Superoxide radical is dismutated by superoxide dismutase and forms H2O2.   O2.-  →   H2O2	Peroxisomses being major site of O2 consumption, in the cell is known to produce H2O2. Damaged peroxisomes release H2O2 into cytosol and yields potent species like .OH.	10
Peroxyl radical (ROO.)	Formed from lipids, proteins, DNA, sugars etc. during oxidative damage.	Highly reactive and participate in peroxide bridged dimer formation and chain reaction.	14, 15
Hydroxy-peroxy radical/ perhydroxy radical  (HOO.)	O2.-+ H+ → HOO.	Simplest peroxyl radical, initiates fatty acid peroxidation, reacts with transient metal ions to yield reactive species.	10, 14
Singlet oxygen (1O2)	Formed during photosensitization and chemical reaction.	Highly reactive, Less stable than normal triplet oxygen.	15, 16

MAJOR DISEASES ASSOCIATED WITH OXIDATIVE STRESS:

Non-controlled production of free radicals has been related to more than 100 diseases including atherosclerosis, cardiovascular diseases, several kinds of cancer, cirrhosis, diabetes, lung diseases, neurological disorders (Alzheimer`s disease, mild cognitive impairment, Creutzfeldt-Jacob disease, meningoencephalitis), Parkinson`s disease, senile and drug induced deafness etc. Excellent reviews on effect of free radicals on diseases have been published by Valko et al (2007) and Rai et al (2011)^{10, 21}.

 

The brain is particularly vulnerable to oxidative damage because of its high oxygen utilization. Oxidative stress increases with age and therefore it can be considered as an important causative factor in several neurodegenerative diseases, typical for older individuals. Under physiological conditions, about 1-3% of the oxygen molecules in the mitochondria are converted into superoxide. The primacy site of radical oxygen damage from superoxide radical is mitochondrial DNA (mt DNA)²². The cell repairs much of the damage done to nuclear DNA, but mt DNA cannot be readily fixed. Therefore, extensive mt DNA damage accumulates over time and shuts down mitochondria, causing cells to die and the organism to age. An interesting correlation between oxygen consumption and ageing was found, i.e. more oxygen consumption, lesser the life spans¹⁰.

 

ENDOGENOUS ANTIOXIDANT DEFENCES:

Antioxidants help organism to deal with oxidative stress. There are many different antioxidant defences in organism. These include enzymatic defences such as superoxide dismutase (SOD), glutathione peroxidases, catalase etc. and non-enzymatic defences like ascorbic acid (vitamin C), α-tocopherol (vitamin E), glutathione, carotenoids, flavonoids etc.²³. Ali et al (2008) showed mechanism of action of these defences in their review article. It is possible to reduce the risks of diseases by enhancing the body`s natural antioxidant defences²⁴. Antioxidants neutralize free radicals by donating one of their own electrons, ending the electron-stealing reaction. The antioxidant nutrients themselves do not become free radicals by donating on electron because they are stable in either form. They act as scavengers, helping to prevent cell and tissue damage that could lead to cellular damage and disease^{25, 26}.

 

MUSHROOM AS ANTIOXIDANT:

Mushrooms are well known for its nutritional and medicinal value^27-31. In Asia mushrooms are used as important source of home remedy to protect human body from various diseases elicited by oxidative stress³². Many edible mushrooms (mostly Basidiomycetes) are good sources of carbohydrates such as β-glucans; phenolics such as tocopherols; B-vitamins such as niacin, flavin and pyridoxine; organic acids such as ascorbate, shikimate, malate and fumarate; monoterpenoid and diterpenoid; lipids; proteins such as hydrophobins and trace elements such as selenium^{6, 33, 34}. These substances are found to be responsible for antimicrobial, antitumor, anti-ageing and antioxidant potentials of mushrooms³⁵.

Important antioxidant components of mushroom:

Phenolic compounds are aromatic hydroxylated compounds, possessing aromatic rings with one or more hydroxyl groups³⁶. Polyphenols can act as antioxidant as they can react highly as hydrogen or electron donors, stabilize chain breaking reaction and terminate Fenton reaction³⁷. Phenolic compound can be involved in H₂O₂ scavenging cascade. As a result, diffusion of free radicals is sterically hindered and peroxidation reactions are restricted³⁸. Positive correlation has been established between total phenolic content in the mushroom extract and their antioxidant activities^39-42. The main phenolic compound found in mushrooms is phenolic acid. Antioxidant activity of phenolic acid is also due to the phenolic hydrogen. It has been found that hydroxyl substitutions at ortho and para position will enhance antioxidant activity. The second hydroxyl group at ortho position results in stronger antioxidant activity than those containing a methoxy substitution ortho to the hydroxyl group. There are a variety of phenolic compounds detected in wild mushrooms such as gallic acid, caffeic acid, quercetin, rutin, vanillin etc.⁸. Paxillus panuoides is found to contain two p-terphenyls which shows potent inhibition effects on lipid peroxidation⁴³.

 

Flavonoids represent a large group of phenolic compounds with antioxidant activity. Flavonoids have been shown to be highly effective scavengers of most types of oxidizing molecules, including singlet oxygen and various free radicals^8. Flavonoids can alter peroxidation kinetics and decrease fluidity of membranes⁴⁴. Generally fungi are not able to produce flavonoids. Exceptionally, flavonoids have been reported in some mushrooms such as Lactarius piperatus⁴⁵.

 

Tocopherols and tocotrienols are essential components of biological membrane⁴⁶. There are four tocopherols and tocotrienol isomers such as α-, β-, γ-, δ- . α-tocopherol has the highest antioxidant activity of all tocopherols⁴⁷. α and β- tocopherols are equally effective in quenching singlet oxygen physically⁴⁸. In membrane, α tocotrienol is found to be better antioxidant than α-tocopherol⁴⁹.

 

Vitamin E is a chain breaking antioxidant⁵⁰. During lipid peroxidation peroxyl radicals are formed from polyunsaturated fatty acids in membrane phospholipids. Vitamin E donates a hydrogen atom to peroxyl radicals forming a hydroperoxide and a tocopheroxyl radical and ultimately forms more stable adducts⁵¹.

 

In recent years, polysaccharide from the fruit bodies of mushroom have earned attention as they can affect a broad spectrum of therapeutic properties including immune-stimulatory, anti-tumour, anti-inflammatory, antifungal, antioxidant and free radical scavenger⁵². In general, the antioxidant properties of polysaccharides are influenced by chemical characteristics like molecular weight, degree of branching, types of monosaccharides, ratio of monosaccharides, intermolecular associations of polysaccharides, glycosidic branching and modification of polysaccharides. Lo et al (2011) reported that among the monosaccharides, rhamnose as the most important determinant factor associated with antioxidant properties. They also found arabinose 1→ 4 and mannose 1→ 2 linkages of the side chain to be significantly related to the reducing power whereas the glucose 1→ 6 linkage and arabinose 1→ 4 linkages are related to scavenging DPPH radicals⁵³. Recently Chen et al (2008) extracted a water soluble protein bound polysaccharide from the fruiting bodies of Ganoderma atrum that contains mannose: galactose: glucose (1: 1.28: 4.9) with an average molecular weight of 1013 kDa and exhibits strong antioxidant activity⁵⁴. The most bioactive mushroom polysaccharides are β-(1→ 3) (1→ 6) glucans⁵⁵. Homo and hetero glucans with β (1→ 3), β (1→ 4) and β (1→ 6) glucosidic linkages are supposed to play a key role in some healthy properties of mushrooms⁵⁶. Kozarski et al (2011) found a correlation between EC₅₀ values of the chelating and reducing power abilities and the amount of total glucans content in crude polysaccharide isolated from Agaricus bisporus, A. brasiliensis, Phellinus linteus and Ganoderma lucidum⁵⁷. A strong correlation was also found between reducing power and total amount of phenols and α-glucans in case of G. applanatum, G. lucidum, Lentinus edodes and Trametes versicolor crude polysaccharide⁵⁸. Polysaccharide can be chemically modified through sulfation, acetylation, phosphorylation or can be purified which could affect antioxidant activity significantly. It has been observed that crude polysaccharide has better antioxidant activity than purified polysaccharide components⁵³. The sulphated derivative of an extracellular polysaccharide (mannogalactoglucan) from Pleurotus sajor-caju showed increased hydroxyl radical scavenging and reducing power⁵⁹. As bioactive polysaccharides exhibit various biological activities affected by different chemical structures it is important to determine the structural and conformational characterization. The chemical structures are studied by FT-IR, liquid state NMR, solid state NMR, Raman spectroscopy, gas chromatography (GC), GC-Mass and HPLC⁶⁰. Polysaccharides can be abstracted by water, alkaline solution and acidic solutions.

 

The EC₅₀ (concentration of extract required for 50% inhibition of free radical) values of alcohol extracts of different mushrooms assayed by different antioxidant methods are summarized in table-2. The EC₅₀ values exerted by polysaccharide isolated from different mushrooms by different antioxidant assays are summarized below      (table-3).

 

 

 

 

 

Table-2: Summarized EC₅₀ value of alcoholic extract (a= Methanol, b= Ethanol) from different mushrooms

Name of mushroom	EC50 value (mg/ ml)								Ref
	1	2	3	4	5	6	7	8
Agaricus arvensis a			4.20			15.85	48.30		61
Agaricus bisporus a			3.63			9.61	21.39
Agaricus romagnesii a			2.23			6.22	4.36
Agaricus silvaticus a			2.08			5.37	3.72
Agaricus silvicola a			3.24			6.39	14.75
Agaricus arvensis a			2.86			3.50	>5		45
Agaricus bisporus a	0.149					0.139			62
Armillaria mellea b	0.036				0.093	0.107			63
Armillaria mellea b			7.53			17.13	8.94		64
Auricularia auricular b	0.373				0.398				65
Austreus hygrometricus b	0.081	0.358			0.088	0.095	0.377		66
Calocybe gambosa b			11.46			34.60	7.57		64
Clitocybe odora b			3.63			6.77	1.36
Coprinus comatus b			1.47			2.56	1.26
Fistula hepatica b	0.083				0.155	0.123			67
Ganoderma applanatum b	0.267				0.166				68
Hypsizigus marmoreus b	No effect		12	3.19		4.19		4.2	69
Lactarius deliciosus a			3.42			8.52			23
Leucopaxillus giganteus a			1.71			1.44	2		70
Macrocybe gigantea b	0.074	0.350			0.080				71
Meripileus giganteus b	0.073				0.132	0.09			72
Pleurotus squarrosulus a	0.706	8.63	13	1.225		1.5	3.794		73
Polyporus grammocephalus b	0.062				0.137	0.129			74
Ramarea aurea b	0.065				0.105	0.091			75
Russula delica b				4		44			76
Russula griseocarnosa pileus a	7.13		2.05	2.33		11.65			77
Russula griseocarnosa stipe a	11.80		2.60	5.99		13.88
Sarcodon imbricatus a			2.79			1.67	3.97		70
Tricholoma giganteum b		0.551	>2	<1					28
Tricholoma portentosuma			3.12			22.9			23

Notes: Antioxidant assays: 1= Inhibition of hydroxyl radical, 2= Inhibition of superoxide radical, 3= Reducing power, 4= Chelating ability of ferrous ion, 5= Inhibition of lipid peroxidation, 6= DPPH assay, 7= Beta-carotene bleaching assay, 8= Conjugated diene method.

 

 

Table 3: List of EC₅₀ values of crude polysaccharide isolated from cold water as well as hot water of different mushrooms.

Name of mushroom	EC50 value (mg/ ml)								Ref
	1	2	3	4	5	6	7	8
Agaricus bisporus d			14.83	7.8	>20	2			57
Agaricus bisporus d	1.05	1.17	1.35			0.55			78
Agaricus brasiliensis d			3.13	2.04	13.25	0.27			57
Agrocybe sp. c					>10	9.559	12.95		79
Armillaria mellea c	0.219				0.198	0.107			63
Armillaria mellea a	0.389				0.102	0.106
Armillaria mellea d			0.98			3.95	0.87		64
Auricularia auricula d	>2	>2	>2			1.62			78
Auricularia auricula c	0.510				0.572				65
Auricularia auricula a	0.403				0.31
Auricularia auricular-judae c					<10	23.92	27.82		79
Austreus hygrometricus c	0.290	0.532			0.099	0.12	0.633		66
Austreus hygrometricus a	0.209	0.502			0.084	0.098	0.479
Calocybe gambosa d			2.38			7.08	8.17		64
Clitocybe odora d			0.94			3.56	0.27
Coprinus comatus d			4.67			7.31	7.43
Flammulina velutipes d	>2	>2	>2			>2			78
Flammulina velutipes c					>10	39.05	38.8		79
Fistula hepatica c	0.293				0.27	0.118			67
Fistula hepatica a	0.299				0.489	0.12
Ganoderma applanatum c	0.624				0.52				68
Ganoderma applanatum a	0.605				0.441
Ganoderma applanatum d			0.18	3.58	2.07	<0.1			58
Ganoderma lucidum d			0.83	7.34	4.05	0.1
Ganoderma lucidum d			0.67	0.59	7.07	<0.1			57
Ganoderma lucidum c					>10	5.28	7.94		79
Hericium erinaceus c					~10	25.47	8.76
Hypsizigus marmoreus c	19		6.08	0.40		6.48		6.59	69
Hypsizigus marmoreus b	13.75		2.24	0.37		15		3.74
Lentinula edodes c					>10	19.09	8.33		79
Lentinus edodes d			5.37	8.26	8.12	<0.1			58
Lentinus edodes d	1.90	>2	>2			0.53			78
Macrocybe gigantea c	0.081	0.602			0.105				70
Macrocybe gigantea a	0.094	0.472			0.123
Meripilus giganteus b	0.400				0.355	0.116			71
Meripilus giganteus c	0.321				0.197	0.107
Phellinus linteus d			0.47	0.91	7.11	<0.1			57
Pleurotus cystidiosus c					~10	31.5	26.08		79
Pleurotus eryngii c					~10	15.42	24.71
Pleurotus flabellatus c					10	17.86	11.97
Pleurotus florida c					>10	21.23	25.08
Pleurotus ostreatus e	0.943	0.053		~1					80
Pleurotus sajor-caju c					>10	23.1	17.5		79
Pleurotus squarrosulus c	0.268	1.473	1.14	0.075		0.34	0.551		72
Pleurotus squarrosulus b	0.364	1.83	1.33	0.09		0.465	0.555
Polyporus grammocephalus c	0.300				0.179	0.092			67
Polyporus grammocephalus a	0.394				0.362	0.125
Ramarea aurea b	0.305				0.367	0.163			74
Ramarea aurea c	0.225				0.331	0.148
Schizophyllum  commune c					>10	35.66	2.21		79
Schizophyllum  commune d			7.9	4.6		0.6		6.9	81
Termitomyces heimii c					>10	26.84	12.79		79
Trametes versicolor d			2.66	>20	>20	0.23			58
Volvariella volvaceae c	0.086					0.256			82

NOTES: Extraction types: a= Water extract at room temperature, b=Cold water extract, c= Hot water extract, d= Hot water extracted crude polysaccharide, e= Hot water extracted purified polysaccharide.

Antioxidant assays: 1= Inhibition of hydroxyl radical, 2= Inhibition of superoxide radical, 3= Reducing power, 4= Chelating ability of ferrous ion, 5= Inhibition of lipid peroxidation, 6= DPPH assay, 7= Beta-carotene bleaching assay, 8= Conjugated diene method.

ANTIOXIDANT PROPERTIES OF SOME EDIBLE AND MEDICINALLY IMPORTANT MUSHROOMS:

The number of mushrooms on Earth is estimated at 140,000 yet may be only 10% (approximately 14,000 named species) are known⁵⁵. This part focuses on antioxidant activity of some popular edible and medicinally important mushrooms.

 

Agaricus sp:

The antioxidant properties of A. brasiliensis were evaluated using methanol, ethanol, dimethyl sulfoxide and water as solvent and extraction was preceded for a variety of time and temperature. The best condition for extraction of antioxidants is with methanol as solvent at 60°C for 60 mins⁸³.  It has been observed that strains with closed basidiocarps have higher antioxidant activity than with opened basidiocarps because they have higher concentration and diversity of glucans and proteins^{84, 85}. Mourão et al (2011) showed that average antioxidant activity for the closed cap group is 24% higher than opened caps⁸³. The phenolic composition of methanolic extract from A. bisporus is analysed by HPLC and it contains rutin, gallic acid, caffeic acid and catechin. All these contribute to its antioxidant activity⁶².

 

Armillaria mellea:

A. mellea, commonly known as honey mushroom, is pathogenic and grows on living trees and on dead and decaying food material⁸⁶. A. mellea has a strong symbiotic relationship with Gastrodia elata, known as Tian Ma⁸⁷. The antioxidant activity of A. mellea ethanol extract is higher than that of Lycoperdon saccatum which is in accordance with higher content of both trace elements, selenium and zinc⁸⁶. Methanolic extracts from dried mycelia, mycelia-free broth and hot water extracts from dried mycelia by A. mellea submerged cultures show low EC₅₀ values (<10 mg/ml). Their ascorbic acid and total phenol contents are well correlated with the reducing power and the scavenging effect on superoxide anions⁸⁷. Exo-polysaccharide and intracellular polysaccharide extracted from broth and mycelia of A. mellea exhibit powerful antioxidant activity. Average molecular weight of exo- polysaccharide and intracellular polysaccharide are 7.68× 10⁶ Da and 5.65× 10⁶ Da respectively⁸⁸.

 

Auricularia sp:

The black brown mushroom A. auricula (Wood ear, Jews ear, jelly ear fungus) consists of high amount of carbohydrates, proteins and minerals⁸⁹. The polysaccharide of A. auricula consists of a backbone of (1→ 3) β-D-glucans⁹⁰ with various residues such as glucose (72%), mannose (8%), xylose (10%) and fucose (10%)⁹¹. Fan et al (2006) showed polysaccharide of A. auricula has antioxidant activity⁸⁹. One low molecular weight polysaccharide of 2.8 × 10⁴ Da isolated from the fruiting body of  A. polytricha shows hydroxyl radical scavenging activity stronger than vitamin C at the same concentration⁹².

 

Boletus sp:

Boletus is a genus of mushrooms, comprising over 100 species. Heleno et al (2011) have evaluated antioxidant activities of six different mycorrhizal Boletus sp (edible: B. aereus, B. edulis, B. reticulatus; not edible: B. purpureus, B. satanas, B. rhodoxanthus). B. aereus shows highest antioxidant activity which is in agreement to its higher total phenolic content (measured by Folin-Ciocalteu assay) and phenolic acid along with cinnamic acid content (measured by HPLC-DAD). EC₅₀ value for DPPH scavenging activity (0.43 mg/ ml) of B. edulis was lower than that of Indian (1.4 mg/ ml), Taiwanian (~1.5 mg/ ml) and Turkish specimen (~0.5 mg/ ml)⁹³. Antioxidant activities of B. edulis and B. auranticus have been also identified by Vidović et al (2010) using 50% ethanol as solvent. Total phenol as well as hydroxyl radical scavenging activity of B. auranticus (EC₅₀ 0.016 mg/ ml) is higher than B. edulis except reducing power where B. edulis shows higher activity. Variegatic acid is found in both extracts⁹⁴.

 

Ganoderma sp:

The widely distributed Ganoderma applanatum or shelf fungus is a unique woody polyporaceae among all mushrooms as it is consumed for its pharmaceutical value rather than food⁶⁸. G. applanatum polysaccharide have the highest chelating ability of ferrous ion, inhibition of lipid peroxidation and reducing power over that of G. lucidum, Lentinus edodes and Trametes versicolor⁵⁸. G. lucidum is called as marvellous herb or mushroom of immortality as it can enhance longevity⁹⁵.  

 

Grifola frondosa:

G. frondosa (Maitake/ king of mushrooms/ the hen of woods) is a Basidiomycete fungus belonging to the order Aphyllopherales and family Polyporaceae. Total polyphenol as major antioxidant components is found in methanolic extract of G. frondosa⁴. Five groups of polysaccharides isolated from G. frondosa showed antioxidant and free radical scavenging activity. These polysaccharides have molecular mass of 470-1650 kDa and consists of backbone of different types of glucan (β-1,6 and β-1,3)⁹⁶.

 

Hypsizigus marmoreus:

The antioxidative properties of H. marmoreus (Tricholomataceae) are reported by Fu et al 2002⁹⁷, Lee et al 2007⁶⁹, Liu et al 1997⁹⁸. Lee et al (2007) reported that total phenol is mostly found in cold water extract than hot water and ethanolic extract. They also found the cold water extract to be more effective than hot water extract with respect to hydroxyl radical scavenging activity⁶⁹.

 

Lentinula edodes:

L. edodes, commonly known as Shiitake, is the second largest cultivated, most popular edible mushroom in world and native to East Asia. In addition to polyphenolic compounds, several bioactive compounds including polysaccharides, dietary fiber, ergostreol, vitamins B1, B2 and C and minerals have been isolated from the fruiting bodies, mycelia and culture medium of the mushroom³². The antioxidant activity of L. edodes is evaluated by using different extraction techniques and different organic solvents⁹⁹. L. edodes polysaccharides isolated from water, acidic and alkaline solution separately show antioxidant activity through inhibition activity of hydroxyl, ABTS⁺ radical and lipid peroxidation¹⁰⁰. Lo et al (2011) showed that polysaccharide of L. edodes has molecular weight between 1× 10⁴ da to 3× 10⁶ Da with a backbone of (1→ 4)-glucan and side chain of (1→ 6)-glucan. Arabinose (1→ 4) and mannose (1→2) linkages also exist in the polysaccharide⁵³.

 

Pleurotus sp:

Genus Pleurotus comprises about 40 species that are commonly referred to as oyster mushroom¹⁰¹. They are ubiquitous¹⁰². Yim et al (2010) assessed the antioxidative potential and total phenolic content of P. ostreatus water extract and found that the ferric reducing power was significantly higher than BHA and ascorbic acid⁶. Iwaloken et al (2007) found higher phenolic contents and antioxidant capacity in the acetone extract of P. ostreatus than petroleum extract³⁴. Chirinang and Intarapichet (2009) found water extracts of P. ostreatus with higher phenolic content possessed better antioxidant activities than ethanol extract⁴². Kim et al (2009) determined the antioxidant activities of methanolic extracts of oyster mushrooms with different colours. Among them, the extract from yellow strain (P. cornucopiae) showed the highest radical scavenging activity, reducing power, ferrous chelating ability and total phenolic contents over dark-grey strain (P. ostreatus) and pink strain (P. salmoneostramineus)¹⁰³.

 

Scizophyllum commune:

The basidiomycete S. commune is found in every continent except Antarctica. Klaus et al (2011) described the antioxidant properties of hot water extract, hot water extracted polysaccharide and hot alkali extracted polysaccharide which consist of a mixture of polysaccharide and phenols. The monosaccharide composition of each extract is established by ¹H-NMR and TLC. Hot water extract was a mixture of α/β glucose (1:1.3). Hot water polysaccharide was a mixture of α/β glucose (1:1) and α/β mannose (0.6:0.4) vs α glucose. Hot alkaline extract was a mixture of α/β glucose (1:1.65) and α mannose. The hot water extract and hot water extracted polysaccharide showed better results in all antioxidant assays than hot alkali extracted polysaccharide⁸¹.

 

Termitomyces sp:

Termitomyces mushrooms grow symbiotically with termites. Puttaraju et al (2006) evaluated antioxidant activity from 23 species of mushrooms in India using water and methanol as solvents. Among all these varieties T. heimii (commonly known as termite nest fungus) in water extract showed the best antioxidant activity followed by its methanolic extract. Total phenolic content was also higher in water extract than in methanol extract. T. mummiformis also showed great antioxidant potential. HPLC analysis predicted a preponderance of tannic acid, gallic acid, protocatacheuic acid and gentisic acid in both T. heimii and T. mummiformis³⁷. Antiradical and antioxidant activity of methanol extract from six Termitomyces species (T. titanicus, T. aurantiacus, T. letestui, T. clypeatus, T. microcarpus and T. eurhizus) growing in Tanzania were evaluated by Tibuhwa (2012). The highest ability to decrease DPPH radical is showed by T. microcarpus (EC₅₀ < 0.1 mg/ ml) followed by T. letestui (EC₅₀ = 0.14 mg/ ml) while least ability was shown in T. eurhizus (EC₅₀= 0.36 mg/ ml). T. microcarpus also showed high antiradical activity (EAU₅₁₅ 1.48) followed by T. aurantiacus (EAU₅₁₅ 1.43) while the lowest were from T. eurhizus (EAU₅₁₅ 0.7). T. microcarpus contained high amount of phenols, flavonoids and β-carotene¹⁰⁴.

 

Tremella fuciformis:

The main bioactive component of T. fuciformis (snow fungus, white jelly mushroom) is polysaccharide. It consists of a linear backbone of (1→ 3) α-D-mannan with side chains composed of glucuronic acid, xylan and fucose. The ratio of mannose, fucose, xylose and glucuronic acid is (9:1:4:3)^{105, 106}. Wu et al (2008) reported the antioxidant activity of T. fuciformis¹⁰⁴.

 

Tricholoma sp:

Tricholoma matsutake is an ectomycorrhizal parasite mushroom and belongs to Basidiomycotina, Agaricales order and Tricholomataceae. Wang et al (2012) isolated two polysaccharides from the water extract of T. matsutake. One polysaccharide consisted of glucose, xylose, galactose (12.89:1.2:1) with molecular weight of 5.939 kDa. The other polysaccharide consisted of glucose only and has molecular weight of 23.23 kDa¹⁰⁷. Wang et al (2012) isolated three polysaccharides from Tricholoma lobayense and evaluated their antioxidant activity¹⁰⁸. Alcohol extract of T. giganteum possesses better antioxidant activity than water and ethyl acetate extract¹⁰⁹. Antioxidant activity depends on the portion of mushroom. Methanol extract of cap portion from T. portentosum  showed better antioxidant activity than its stipe portion, although both are lower than the entire mushroom²³.

 

CONCLUSION:

In this review, we have focused on comparative antioxidant activity of some edible and medicinally important mushrooms all over the world as well as active ingredients of mushrooms possessing antioxidant properties. We have found that EC₅₀ value of the same mushroom at the same antioxidant assay gives different results as bioactive compounds are released depending upon solvent type, extraction temperature, extraction time, maturation of the mushroom and of course on the environment. There is a strong relationship between amount of phenolic compound, polysaccharide compound in the extract and antioxidant activity. Thus, it is found that the crude polysaccharide gives better result than purified one.  Mushrooms like Austreus hygrometricus, Fistulina hepatica, Phellinus linteus, Pleurotus squarrosulus, Polyporus grammocephalus, Macrocybe gigantea show higher antioxidant potential as presented in tables. To our best knowledge, DPPH is the most common antioxidant assay to be used and Pleurotus sp is one of the most vastly studied mushrooms. It can be concluded that mushrooms have valuable therapeutic potential that can be used for the prevention and control of several diseases.

 

 

 

 

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Received on 15.03.2013       Modified on 01.04.2013

Accepted on 10.04.2013      © RJPT All right reserved