Reactive oxygen species and antioxidant properties from mushrooms.

Preventive medicine and food industry have shown an increased interest in the development of natural antioxidants, since those most commonly used synthetic antioxidants may have restricted use in food. This could explain why there is currently much research on the antioxidant properties from natural products such as mushrooms. Many mushrooms have been reported to possess antioxidant properties, which enable them to neutralize free radicals. The oxygen molecule is a free radical, which lead to the generation of the reactive oxygen species and can damage the cells. Cell damage caused by free radicals appears to be a major contributor to aging and degenerative diseases. Mushrooms antioxidant components are found in fruit bodies, mycelium and culture both, which include polysaccharides, tocopherols, phenolics, carotenoids, ergosterol and ascorbic acid among others. Fruit bodies or mycelium can be manipulated to produce active compounds in a relatively short period of time, which represent a significant advantage in antioxidant compounds extraction from mushrooms. Antioxidant compounds may be extracted to be used as functional additives or mushrooms can be incorporated into our food regime, representing an alternative source of food to prevent damage caused by oxidation in the human body.

Introduction

Mushroom

The term mushroom may come from the Latin word mucus (slime) [1]. According to Chang and Miles [2] “mushroom is a macro fungus with a distinctive fruit body, which can be either epigeous (grow above the earth) or hypogeous (grow underground; i.e. truffles) and large enough to be seen with naked eye to be picked by hand”. These organisms are a very large and diversified group of macrofungi (i.e. higher fungi) belonging to basidiomycetes and ascomycetes that can be edible or non-edible. The fungal spores for these two groups of macrofungi are located in a special structure called basidium (for basidiomycetes) or ascus (for ascomycetes). Mushrooms grow mostly above the earth and some of them have an umbrella-shaped fruiting body, where spores are produced (in lamellae, structures on the underside of the pileus or cap). Two phases of growth are distinguishable in these organisms; the reproductive phase (fruit bodies) and the vegetative phase (mycelia or mycelial growth). During substrate invasion, hyphae continually grow and branch to form a network of hyphae (mycelia) and a fruit body grows from underground mycelia by a process called fructification. Mycelial growth is generally coupled with increased enzyme production and respiration. Hyphae absorb digestive products, penetrating the substrate to some extent. The fungal cell wall can be formed by β-D-glucans, proteins, and chitin (Fig. 1). From the ecological point of view, mushroom can be saprotrophs, parasites and mycorrhiza. There are only few parasitic mushrooms. Most of the cultivated mushrooms are saprotrophs. Mycorrhizal mushrooms have a symbiotic relationship with some vegetation, mainly trees, having a relationship of mutual need. Saprotrophs are able to obtain nutrients from dead organic material and parasites obtain their food from living animals and plants, causing harm to the host [3]. Mushrooms have been eaten and appreciated for their exquisite flavor, economic and ecological values, and medicinal properties for many years. In general, mushrooms contain 90% water and 10% dry matter [4]. They have chemical composition which is attractive from the nutritional point of view [5]. Their nutritional value can be compared to those of eggs, milk, and meat [6]. Mushrooms contain vitamins (thiamine, riboflavin, ascorbic acid, ergosterol and niacin) as well as an abundance of essential amino acids. They also have proteins, fats, ash, and glycosides. Volatiles oils, tocopherols, phenolic compounds, flavonoids, carotenoids, folates, organic acids, etc [7], [8]. The total energetic value of mushroom caps is between 250 and 350 cal/kg of fresh mushrooms [4]. Mushrooms can be considered as functional food which provides health benefits in addition to nutritional value [9]. They have been collected in several countries for hundreds of years and technological improvements have made possible their cultivation world-wide.

Fig. 1

Illustrative representation of fungal cell wall components and stages of mushroom growth.

Reactive oxygen species and antioxidant system

Around 2.45 billions of years ago molecular oxygen was introduced in our environment by the O2-evolving photosynthetic organisms and reactive oxygen species (ROS) has been present ever since in aerobic life [10]. The O2 molecule is a free radical (it has two impaired electrons), which lead to the generation of the ROS and can damage the cells of all organisms. A free radical is a chemical compound that contains one or more unpaired electrons in atomic or molecular orbitals [11]. Reactive molecules such as superoxide anion (O2•−), hydroxyl radical (OH•), hydroxyl ion (OH−), nitric oxide (NO•) and hydrogen peroxide (H2O2) are free radicals and non-radical molecular forms, respectively derived from molecular oxygen. In humans, oxidation is a process that the body uses for normal energy production and immune function. This is part of the process that enables the body to transform nutrients such as carbohydrates, fats, and proteins into energy. During oxidation, ROS are produced at low levels in normal physiological conditions, which are necessary for maintaining normal cell functions, and the endogenous antioxidant defense systems of the body have the capacity to avert any harmful effects. However, ROS are extremely harmful to organisms at high concentrations. When the level of ROS exceeds the defense mechanisms, they can affect many cellular functions by damaging nucleic acids, oxidizing proteins, and causing lipid peroxidation (Fig. 2). ROS can be produced either by external sources (e.g. tobacco smoke, ozone, stress, etc.) or as byproducts during the mitochondrial electron transport of aerobic respiration or by oxidoreductase enzymes and metal catalyzed oxidation [12]. Because they are reactive, radicals search out ways of pairing up their electron, so radicals often attack nearby chemical compounds. These chemical compounds may be involved in important enzyme reactions, may be components of cell walls or may be part of a DNA molecule. If their chemical structure is changed, their function in the cell may be lost and the result can be cellular senescence or apoptosis [12]. Cell damage caused by free radicals appears to be a major contributor to aging and degenerative diseases of aging such as cancer, cardiovascular disease, cataracts, immune system decline, liver diseases, diabetes mellitus, inflammation, renal failure, brain dysfunction and stress among others [11], [13] (Fig. 2). Neutralizing of free radicals or peroxide radicals by an antioxidant agent is important for cell protection against oxidative stress. Then, antioxidants are chemicals which inhibit the oxidation reaction of free radicals by exchanging one of their own electrons with the free radical molecules to stabilize them. These compounds can be endogenous and dietary antioxidants such as polyphenol, vitamin A (e. g. carotenoids), vitamin E (α-tocopherol), β-glucan, etc. Proteins and low molecular weight antioxidants such as ascorbic acid (vitamin C), glutathione, etc, are endogenous antioxidants. Glutathione may be the most important intra-cellular defense against the deleterious effects of ROS. It is a tripeptide (glutamyl-cysteinyl-glycine), which provides an exposed sulfhydryl group as target for attack. Metal-binding proteins and enzymes are antioxidant proteins. Enzymes that can fight free radical formation and propagation are superoxide dismutase, glutathione peroxidase, etc, and enzymes that repair or eliminate damage biomolecules include lipase, peptidase, transferase among others [14], [15] (Fig. 3).

Fig. 2

Schematic representation of a human cell, which can be damaged by free radicals generated from internal and external sources. Neutralizing of free radicals by an antioxidant agent is important to maintain a healthy cell.

Fig. 3

Schematic representation of antioxidant system and antioxidant molecules.

In vitro methods to assess antioxidant activity

Around 11 in vitro methods have been used for antioxidant evaluation activity in a biological material [16]. The most commonly used methods to measure mushrooms antioxidant activity are those involving chromogen compounds of radical nature that stimulate the reductive oxygen species (e.g. ABTS and DPPH methods). Examples of other methods that are also used are mentioned below.

DPPH• and ABTS•+ assays

DPPH• assay is based on scavenging of the purple chromogen radical 1,1-diphenyl-2-picrylhydrazyl (DPPH•) by the antioxidants, which produces a decrease in absorbance at 515 nm. When a solution of DPPH• is mixed with a substance that can donate a hydrogen atom, the reduced form of the radical is accompanied by loss of color. The activity is expressed as half inhibitory concentration IC50. It refers to the amount of antioxidant necessary to decrease by 50% the initial DPPH• concentration. Therefore, a lower IC50 means better radical scavenging activity or antioxidant activity [16], [17].

2,2′;-azinobis-(3-ethylbenzothiazoline-6-sulphonate) radical cation (ABTS•+) assay is also known as Trolox equivalent antioxidant capacity (TEAC) assay. The antioxidant reduces ABTS•+ to ABTS and decolorize it. The relative ability of hydrogen-donating antioxidants to scavenge ABTS•+ can be measured spectrophotometrically at 734 nm. Results are expressed by comparison with standard amounts of the synthetic antioxidant trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid), a water-soluble analog of vitamin E that can be used as an antioxidant standard to give rise to the TEAC [16].

Superoxide anion radical scavenging activity assay

Superoxide anion (O2•−), resulting from the univalent reduction of O2, is considered as being the first step leading to oxidative stress. For measuring O2•− scavenging activity, a suitable system should be selected for generating these radicals. Two systems are used for producing O2•−; the xanthine/xanthine oxidase system and phenazine methosulphate system in the presence of nicotinamide adenine dinucleotide (NADH). The reaction of formation of O2•− is based on the catalysis of xanthine oxidase. In this case, nitroblue tetrazolium (NBT), a probe/target for measuring the O2•− scavenging capacities of samples is used. The color reaction of the O2•- with NBT is detected at 560 nm. Antioxidant activity of samples to inhibit the color to 50% is measured in terms of IC50 [16], [18].

Reducing power method

This method is based on the principle of increase in the absorbance of the reaction mixtures. Increase in the absorbance indicates the reducing power of the samples (antioxidant activity). In this method, antioxidant compound forms a colored complex with potassium ferricyanide, trichloro acetic acid and ferric chloride, which is measured at 700 nm [19].

Ferrous ion chelating assay

The interaction of ferrous ion (Fe2+) with hydrogen peroxide in biological systems can lead to formation of highly reactive hydroxyl radicals. Ferrozine is a ferroin compound that can form a complex with a red color by forming chelates with Fe2+. In the presence -of other chelating agents, the complex formation is disrupted, resulting in a decrease of the red color of the ferrozine-Fe2+ complexes. Measurement (spectrophotometrically at 562 nm) of the rate of color reduction therefore allows estimation of the chelating activity of the coexisting chelator. The chelation of ferrous ions is determined using the method of Dinis et al. [20]. EDTA is used as a reference standard for this assay. A lower absorbance value indicates a better ferrous ion-chelating ability of the test sample.

Antioxidant compounds from mushrooms

A wide range of mushrooms have been reported to possess antioxidant properties. Extracts from mushrooms contain many components, each of which is unique of a specific mushroom. Antioxidant compounds are found in fruit bodies, mycelium and culture both, which can be phenolics, polysaccharides, tocopherols, flavonoids, carotenoids, glycosides, ergothioneine and ascorbic acid (Table 1).

Table 1

Antioxidant compounds in mushrooms.

Mushroom scientific name	Mushroom common names	Phyllum/Edibility	Antioxidant compounds	Biomaterial source	Reference
Agaricus arvensis	Horse mushroom	B/E	β-Carotene, ascorbic acid, lycopene, phenolic compounds	Fruit bodies extracts	[42], [43], [44]
Agaricus bisporus	Common mushroom, button mushroom, white mushroom, champignon mushroom	B/E	Pyrogalloll-ergothioneine,α- and β-glucansCatechin, gallic acid,rutin, caffeic acid	Fruit bodies and myceliaFruit bodies hot water extracts	[17], [33], [35], [44], [45], [46], [47], [48], [49]
Agaricus blazei	Almond mushroom, mushroom of the sun	B/E	Benzoic acid, myricetin, quercetin, pyrogallolα- and β-Glucans	Fruit bodies hot water extractMycelia extracts	[17], [35], [50]
Agaricus romagnesii	NA	B/NE	Phenolic compounds, β-carotene	Fruit bodies	[43], [44]
Agaricus silvaticus	Scaly wood mushroom	B/E	Phenolic compounds, β-carotene	Fruit bodies	[43], [44]
Agaricus silvicola	Wood mushroom	B/E	β-Carotene, ascorbic acid, lycopene, phenolic compounds	Fruit bodies extracts	[42], [44], [45]
Agrocybe cylindracea	Black poplar mushroom	B/E	α-Tocopherol, β-tocopherol	Fruit bodies	[32], [51]
Amanita rubescens	blusher	B/NE	Phenolics compounds, flavonoids	Methanolic extract	[33], [52]
Armillaria mellea	Honey mushroom	B/NE	Antioxidant components, ascorbic acid, flavonoids and phenolic compounds	Dried mycelia and mycelia-free broth extracts	[53]
Armillaria ostoyae	Humongous fungus	B/NE	Phenolic compounds	Fruit bodies extracts	[33]
Auricularia auricula-judae	Jelly mushroom; judas's ear fungus	B/E	Polysaccharides, phenolic compounds	Fruit bodies	[40], [54]
Auriculariapolytricha	Cloud ear, jelly ear	B/E	Phenolic compounds	Fruit bodies extracts	[34], [55]
Boletus badius	Bay bolete	B/E	β-Carotene, α-tocopherol,phenolic compounds, flavonoids	Fruit bodies methanolic extracts	[36], [49], [56], [57]
Boletus edulis	Porcini, penny bun	B/E	β-Carotene, ascorbic acid, flavonoids, tocopherols	Fruit bodies extracts	[34], [47], [49], [56], [58], [59]
Calocybe gambosa	St. George's mushroom	B/E	Phenolic compounds, flavonoids	Fruit bodies methanolic extracts	[47]
Cantharellus cibarius	Chanterelle	B/E	Phenolic compounds, flavonoids	Fruit bodies extracts	[34], [45], [47], [49], [52]
Cantharellus clavatus	Pig's ears, violet chanterelle	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Chlorophyllum rhacodes	Shaggy parasol	B/NE	Phenolic compounds	Fruit bodies extracts	[33]
Clavaria vermicularis	Fairy fingers, white worm coral	B/E	Flavonoids, ascorbic acid	Fruit bodies methanolic extracts	[25]
Clitocybe alexandri	Alexander's Funnel	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36], [60]
Clitocybe geotropa	Trooping funnel	B/E	Phenolic compounds	Fruit bodies extracts	[61]
Coprinopsis atramentaria	Common ink cap, inky cap	B/NE	β-Glucans	Fruit bodies extract	[48]
Coprinus comatus	Shaggy ink cap	B/E	β-Carotene, ascorbic acid, lycopene, phenolic compounds	mycelium ethanolic extract	[62]
Coriolus versicolor	Polypore mushroom	B/NE	Gallic, p-coumaric, protocatechin, caffeic and vanillc acids	Methanolic extracts	[63]
Cortinarius glaucopus	Blue-foot webcap	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Craterellus cornucopioides	Horn of plenty	B/E	Phenolic compounds, flavonoids	Fruit bodies methanolic extracts	[47]
Fistulina hepatica	Beefsteak fungus, beefsteak polypore	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Flammulina velutipes	Golden needle mushroom; enokitake (Japanese name)	B/E	Gallic acid, pyrogallol, homogentisic acid, 5-sulfosalicylic acid, protocatechuic acid, quercetin, caffeic acid	Fruit bodies methanolic extractsMycelium extracts	[35], [64], [65]
Ganoderma applanatum	Artist's bracket, artist's conk, bear bread	B/NE	Gallic, p-coumaric, protocatechin, caffeic and vanillc acids	Methanolic extracts	[63]
Ganoderma lucidum	Lingzhi mushroom, Reishi (Japanese name)	B/E	Quercetin, kaempferol,Triterpenoids, polysaccharides	Fruit bodiesMycelium	[17], [55], [66]
Ganoderma tsugae	Hemlock varnish shelf	B/NE	Polysaccharides	Fruit bodies, mycelia and extracts	[67]
Gomphus clavatus	Pig's ears, violet chanterelle	B/E	Ergosterol, phenolic compounds	Fruit bodies extracts	[68]
Grifola frondosa	Hen-of-the-woods, ram's head and sheep's head.	B/E	Phenolic compounds,β-1,6 and β-1,3-glucan	Fruit bodies extract	[69], [70]
Helvella crispa	White saddle, elfin saddle, common helvel	A/NE	Phenolic compounds	Fruit bodies extracts	[34]
Hericium erinaceus	Lion's mane mushroom,	B/E	Phenolic compounds	Fruit bodies and mycelium extract	[71]
Hydnum repandum	Sweet tooth, wood hedgehog, hedgehog mushroom	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[33], [34], [36], [72]
Hygrophoropsis aurantiaca	False chanterelle	B/NE	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Hygrophorus marzuolus	March mushroom	B/E	Phenolic compounds, flavonoids	Fruit bodies methanolic extracts	[47]
Hypholoma capnoides	NA	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Hypholoma fasciculare	Sulphur tuft, sulfur tuft,	B/NE	Tocopherols, phenolics, flavonoids, ascorbic acid, β-carotene	Fruit bodies extracts	[42]
Hypsizygus marmoreus	Brown Beech Mushroom	B/E	Ascorbic acid, β-carotene, tocopherols	Fruit bodies methanolic extracts	[73]
Inonotus obliquus	Chaga mushroom	B/E	p-Hydroxybenzoic acid, quercetin, kaempferol	Mycelium; methanolic and water extracts	[35], [55]
Laccaria amethystine	Amethyst deceiver	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Laccaria laccata	The deceiver, waxy laccaria	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Lactarius aurantiacus	NA	B/NE	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Lactarius citriolens	NA	B/NE	Free sugars, fatty acids, tocopherols and phenolic acids	Fruit bodies methanolic extracts	[74]
Lactarius deliciosus	Saffron milk cap and red pine mushroom	B/E	Phenolic compounds, flavonoids	Fruit bodies extracts	[33], [34], [43], [47], [75]
Lactarius piperatus	Peppery milk-cap	B/E	Phenolic compounds, flavonoids	Methanolic extract	[33], [52], [76]
Lactarius salmonicolor	Milky agaric	B/E	Phenolic compounds	Methanolic extract	[33], [77]
Lactarius sanguifluus	Bloody milk cap	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Lactarius turpis	Ugly milk-cap	B/NE	Free sugars, fatty acids, tocopherols, phenolic acids	Fruit bodies methanolic extracts	[74]
Lactarius volemus	The weeping milk cap	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Laetiporus sulphureus	Crab-of-the-woods, sulphur polypore	B/E	Gallic, p-coumaric, protocatechin, caffeic and vanillc acids	Methanolic extracts	[63]
Leccinum scabrum	Rough-stemmed bolete	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Leccinum spp	NA	B/NE	Phenolic compounds, β-carotene, lycopene	Aqueous and methanolic extracts of dried fruiting bodies	[49]
Lentinula edodes	Forest mushroom, shiitake	B/E	Gallic acid, protocatechuic acid, catechin, tocopherols	Fruit bodiesFruit bodies extracts	[35], [78], [59], [55], [64]
Lentinus squarrolosus	NA	B/E	β-Carotene, lycopene, flavonoids	Fruit bodies extracts	[79]
Lenzites betulina	Gilled polypore	B/E	Betulinan A, B Benzoquinone	Fruit bodies extracts	[79]
Lepista inversa	NA	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36], [60]
Lepista nuda	Wood blewit, blue stalk mushroom	B/E	β-Carotene, α-tocopherol	Fruit bodies methanolic extracts	[56], [75]
Lepista sordida	Fairy rings	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Leucopaxillus giganteus	Giant leucopax	B/E	β-carotene, ascorbic acid, lycopene, phenolic compounds	Fruit bodies extracts	[75]
Lycoperdon molle	The smooth puffball	B/E	Phospoethanolamida, lysophosphatidyl choline	Fruit bodies extracts	[26], [80]
Lycoperdon perlatum	Common puffball	B/E	Flavonoids, ascorbic acid	Fruit bodies methanolic extracts	[45], [25]
Macrolepiota mastoidea	NA	B/E	Tocopherols, phenolics, flavonoids, ascorbic acid, β-carotene	Fruit bodies extracts	[75]
Macrolepiota procera	The parasol mushroom	B/E	Phenolic compounds	Fruit bodies extracts	[75], [33], [34], [40], [49]
Marasmius oreades	Scotch bonnet, fairy ring mushroom	B/E	Flavonoids, ascorbic acid	Fruit bodies methanolic extracts	[25]
Meripilus giganteus	Giant polypore, black-staining polypore,	B/E	Gallic, p-coumaric, protocatechin, caffeic and vanillc acids	Methanolic extracts	[63]
Mycena rosea	Rosy bonnet	B/NE	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Panus conchatus	Lilac oysterling	B/NE	Phenolic compounds, flavonoids	Fruit bodies	[40]
Panus tigrinus	NA	B/NE	Gallic, p-coumaric, protocatechin, caffeic and vanillc acids	Methanolic extracts	[63]
Phellinus igniarius	Willow bracket, fire sponge	B/NE	Hispidin	Dried mushrooms	[81]
Phellinus linteus	Black hoof mushroom, meshimakobu (Japanese name)	B/NE	β-Tocopherol, protocatechuic acid,gallic acid; pyrogallol; homogentisic acid,α- and β-glucans	Fruit bodiesmethanolic andethanolic extractsFruit bodies hot water extract	[35], [17], [82]
Pleurotus albidus	NA	B/E	Phenolic compounds	Mycelium extracts	[83]
Pleurotus cornucopiae	NA	B/E	Phenolic compounds	Fruit bodies extracts	[61]
Pleurotus cystidiosus	Abalone oyster; summer oyster mushroom	B/E	Tocopherols	Fruit bodies methanolic extracts	[64]
Pleurotus djamor	Pink oyster mushroom	B/E	Phenolic compounds	Fruit bodies extracts	[34], [84]
Pleurotus dryinus	NA	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Pleurotus eous	NA	B/E	Flavonoids	Fruit bodies water extracts	[85]
Pleurotus eryngii	King oyster, king trumpet mushroom;	B/E	Gallic acid, protocatechuic acid, naringin, kaempferol, rutin, resveratrol, catechin	Fruit bodies methanolic extracts	[45], [86]
Pleurotus ostreatus	Oyster mushroom	B/E	β-Glucans,gallic acid, homogentisic acid, naringin, myricetin, tocopherols,glycoproteins, β-D-Glucan (pleuran) Lectin	Fruit bodies methanolic extracts	[35], [49], [61], [62], [64], [81], [87]
Pleurotus pulmonarius	Indian oyster, italian oyster, phoenix mushroom	B/E	Flavonoids, ascorbic acid	Fruit bodies methanolic extracts	[25], [81]
Pleurotus sajor-caju	Grey oyster mushroom	B/E	Phenolic compounds	Fruit bodies water and methanolic extracts	[34], [88]
Polyporus squamosus	Dryad's saddle and pheasant's back mushroom	B/NE	β-Carotene, α-tocopherol	Fruit bodies methanolic extracts	[56]
Polyporus tenuiculus	NA	B/E	Phenolic compounds	Fruit bodies	[40]
Pycnoporus sanguineus	NA	B/NE	Phenolic compounds	Mycelium extracts	[80]
Ramaria botrytis	Clustered coral, the pink-tipped coral mushroom	B/NE	Tocopherols, phenolic compounds, ascorbic acid, β-carotene	Fruit bodies extracts	[26]
Ramaria formosa	Beautiful clavaria, pink coral fungus	B/NE	Ascorbic acid, flavonoids	Fruit bodies extracts	[25]
Russula brevipes	Short-stemmed russula, the stubby brittlegill	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Russula cyanoxantha	Charcoal burner	B/E	Phenolic compounds	Methanolic extract	[52]
Russula delica	Milk-white brittlegill	B/E	β-carotene, α-tocopherolphenolic compounds	Fruit bodies methanolic extracts	[33], [56]
Russula integra	The entire russula	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Russula nigricans	Blackening brittlegill	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Russula vesca	Bare-toothed russula	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Russula vinosa	Darkening brittlegill	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Sarcodon imbricatus	Shingled hedgehog, scaly hedgehog	B/E	β-Carotene, ascorbic acid, lycopene, phenolic compounds	Fruit bodies extracts	[42], [75]
Schizophyllum commune	Split-gill fungus	B/NE	α- and β-Glucans, phenolic compounds	Fruit bodies extracts	[89]
Sparassis crispa	Cauliflower fungus	B/E	Protocatechuic acid, benzoic acid, p-hydroxibenzoic acid	Fruit bodies	[35], [72]
Suillus bovinus	Jersey cow mushroom, bovine bolete	B/E	Phenolic compounds, β-carotene	Aqueous and methanolic extracts of dried fruiting bodies	[49]
Suillus collinitus	NA	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Suillus luteus	Slippery jack or sticky bun	B/E	Phenolic compounds	Fruit bodies extracts	[33]
Suillus mediterraneensis	NA	B/E	Tocopherols, phenolic compounds	Fruit bodies extracts	[36]
Suillus variegatus	Velvet bolete	B/E	Phenolic compounds, β-carotene	Aqueous and methanolic extracts of dried fruiting bodies	[49]
Termitomyces heimii	Termite nest fungus	B/E	Phenolic compounds	Fruit bodies extracts	[34], [66]
Termitomyces microcarpus	NA	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Termitomyces mummiformis	NA	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Termitomyces schimperi	NA	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Termitomyces tylerance	N/A	B/E	Phenolic compounds	Fruit bodies extracts	[34]
Tremella fuciformis	White jelly fungus, white wood ear, snow mushroom	B/E	3,4-dihydroxybenzaldehyde, vanillic acid, caffeic acid, syringic acid and 3,4-dihydroxybenzlacetone	Ethanolic and water extracts	[55]
Tricholoma acerbum	Bitter knight	B/E	Tocopherols, phenolic compounds, ascorbic acid, β-carotene	Fruit bodies extracts	[26]
Tricholoma equestre	Man on horseback, Yellow knight	B/NE	Phenolic compounds, β-carotene	Aqueous and methanolic extracts of dried fruiting bodies	[49]
Verpa conica	Bell morel, the thimble fungus	A/NE	β-Carotene, α-tocopherol	Fruit bodies methanolic extracts	[56]
Volvariella volvaceae	Paddy straw mushroom	B/E	Phenolic compounds	Fruit bodies extracts	[66]
Xerocomus subtomentosus	Suede bolete, boring brown bolete	B/E	Phenolic compounds, β-carotene	Aqueous and methanolic extracts of dried fruiting bodies	[49]

B: Basidiomycota, A: Ascomycota, E: Edible, NE: Non-edible, NA: not available.

Phenolic compounds

Phenolic compounds are aromatic hydroxylated compounds with one or more aromatic rings and one or more hydroxyl groups. They include phenolic acids, flavonoids, hydroxybenzoic acids, hydroxycinnamic acids, lignans, tannins, stilbenes and oxidized polyphenols. Furthermore, some of them stimulate synthesis of endogenous antioxidant molecules in the cell [21], [22]. It has been reported that phenolic compounds exhibit antioxidant activity in biological systems, acting as free radical inhibitors, peroxide decomposers, metal inactivators or oxygen scavengers [23], [24]. Phenolic compounds are present in all the mushrooms. These compounds can be pyrogallol, myricetin, caffeic acid, quercetin and catechin among others (Table 1). Mushrooms contain large amounts of polyphenols at concentrations in the range of 6.25–3.62 mg/mL [25], [26]. It has been reported that grapes and wine contain between 1.0 and 1.8 μg/mL of these compounds [27].

Polysaccharides

A glucan is a d-glucose homopolysaccharide linked by glycosidic bonds. Glucans are classified as α-or β-glucans according to types of glycosidic bonds. α-Glucans are mainly present for storage of glucose such as starch, glycogen, and dextran. β-Glucan is a non-starch polysaccharide comprised of β-linked d-glucose molecules linked to one another by 1–3 glycosidic chain with 1–6 glycosidic branches. The physicochemical properties of β-glucans differ depending on characteristics of their primary structure, including linkage type, degree of branching, molecular weight, and conformation (e.g., triple helix, single helix, and random coil structures) [28], [29]. β-Glucan is one of the key components of the fungal cell wall (Fig. 1). Hence, antioxidant properties of mushrooms are mainly attributed to β-glucans [13]. Trznadel et al. [30] reported an increase of superoxide dismutase when the commercial yeast β-glucan (Zymosan®) was administrated to chronic uremic patients. Superoxide dismutase is one of the basic antioxidant enzymes we have that fight free radicals (Fig. 3). The length and branches of fungal β-glucan from various mushrooms is widely different [31].

Ascorbic acid

l-ascorbic acid (vitamin C), being water-soluble, can work inside and outside the cell to combat free radical damage. Vitamin C has been detected in several mushrooms. Among them Boletus edulis [32], B. pseudosulphureus) [33], Lactarius deliciosus [34], Pleurotus ostreatus [35], Suillus luteus [36] among others. Ramesh and Pattar [25] reported that mushrooms contain vitamic C at concentrations in the range of 0.15–0.06 mg/mL. Orange juice contains around 0.37 mg of vitamic C/mL [37].

Tocopherols

Vitamin E is a common term for eight different compounds; four tocopherols (α-, β-, γ-, and δ-tocopherol) and four tocotrienols. Among them α-tocopherol is the most biologically active. This fat-soluble compound is embedded within the cell membrane, which has a protective fatty layer of lipids [13]. In this way, α-tocopherol can disable free radicals. Tocopherols have been detected in most mushrooms (Table 1).

β-carotene and lycopene

β-carotene and lycopene are carotenoids, which are natural pigments present in food (e. g. vegetables, fruits and mushrooms) but are not synthetized by animals. β-carotene is the precursor for the synthesis of vitamin A. Lycopene is an acyclic isomer of β-carotene, and has no vitamin A activity. It is a highly unsaturated, straight chain hydrocarbon containing conjugated and two non-conjugated double bonds, which makes it a potent antioxidant [38], [39]. Hussein et al. [40] reported that the amount of β-carotene and lycopene detected in Lentinus squarrolosus, were in abundance compared to the concentration reported in some vegetables (e.g. carrot, persimmon and tomato) (Table 1).

Ergosterol

Some mushrooms possess ergosterol (Table 1), which is the precursor of vitamin D. In mushrooms, ergosterol is converted to vitamin D2 (ergocalciferol) when exposed to UV radiation. Vitamin D2 serves as the only available dietary source of vitamin D for those who eat no animal products. Vitamin D is crucial for bone health [41].

Concluding remarks

Mushrooms are a natural source of food and antioxidant are becoming important in human health. Interestingly, antioxidant potential in mushrooms is higher than in most vegetables and fruits. The consumption of dietary antioxidant will protect against free radical damage for the prevention of various diseases and aging. Technological developments in cultivation technologies make it possible to produce a wide variety of mushrooms. In addition, research into devising method for cultivation of wild mushrooms is being carried out, so these organisms can be cultivated through artificial methods. A significant advantage in antioxidant compounds extraction from mushrooms is that fruit bodies or mycelium can be manipulated to produce active compounds in a relatively short period of time. Antioxidant compounds may be extracted to be used as functional ingredients or mushrooms can be incorporated to our diet to help the human body to reduce oxidative damage. Health benefits and delicious taste of mushrooms make them a good choice of food to include in our food regime.