Wild edible mushrooms as an alternative for the consumption of antioxidants and phenolic compounds: An overview

Abstract

Fungi are a diverse group, and they are essential for health, the economy, and food. Interest in these organisms has increased because of the importance and effect of their chemical components viz., phenolic compounds, which are considered an alternative source of antioxidants. Antioxidants are compounds that prevent cell damage and can help prevent or counteract certain diseases (cardiovascular, neurodegen-erative, cancer, etc.) because they can improve cell function (changes in enzyme activity, enzyme patterns, membrane fluidity, and responses to stimuli), among others. To date, no adverse side effects have been reported. The difference in production is due to several factors, such as the growth environment, nutrition, cell age, the part from where the phenolic compounds are obtained (pileus, stipe, or mycelium), the extraction method, etc. This article aims to provide an overview of wild edible mushrooms, to promote the study of their antioxidant capacity, and to better understand the nutraceutical potential of edible mushrooms consumed in different parts of the world.

Full Article

Wild Edible Mushrooms as an Alternative for the Consumption of Antioxidants and Phenolic Compounds: An Overview

Maura Téllez-Téllez *

Fungi are a diverse group, and they are essential for health, the economy, and food. Interest in these organisms has increased because of the importance and effect of their chemical components viz., phenolic compounds, which are considered an alternative source of antioxidants. Antioxidants are compounds that prevent cell damage and can help prevent or counteract certain diseases (cardiovascular, neurodegen-erative, cancer, etc.) because they can improve cell function (changes in enzyme activity, enzyme patterns, membrane fluidity, and responses to stimuli), among others. To date, no adverse side effects have been reported. The difference in production is due to several factors, such as the growth environment, nutrition, cell age, the part from where the phenolic compounds are obtained (pileus, stipe, or mycelium), the extraction method, etc. This article aims to provide an overview of wild edible mushrooms, to promote the study of their antioxidant capacity, and to better understand the nutraceutical potential of edible mushrooms consumed in different parts of the world.

DOI: 10.15376/biores.19.2.Tellez-Tellez

Keywords: Antioxidant; Oxidative stress; Oxidation prevention; Ecological importance; Phenolic acids; Wild mushrooms

Contact information: Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Morelos, México; *Corresponding author: maura.tellez@uaem.mx

INTRODUCTION

The macrofungus presents a distinctive fruiting body large enough to be seen with the naked eye (DaSilva 2005). Wild fungi are essential within the structure and functioning of the ecosystem. Saprotrophic fungi are the primary agents of decomposition of organic matter, releasing CO₂ and mineral nutrients, increasing soil fertility. Symbiotic fungi are the leading suppliers of nutrients for plants and receive in exchange the vegetable carbon derived from photosynthesis (Hawkins et al. 2023). Ectomycorrhizal fungi maintain efficient communication with plants and other microorganisms through a mycelial network and the exchange of nutrients, water, and defense compounds. Parasitic fungi regulate the structure of communities, maintaining biodiversity by limiting the dominance of any species within an ecosystem (Pérez-Moreno et al. 2021).

The role of wild fungi in nutrient recycling is of great ecological importance (Niego et al. 2023). Clemmensen et al. (2013, 2015) indicated that fungi have multifunctionality in the ecosystem (organic matter mineralization, climate regulation, and nutrient cycling). This is because of the production of a wide variety of extracellular enzymes that can break down organic matter, thus regulating carbon balance (between 40 to 55%), with production of carbon dioxide and organic acids. Moreover, via degradation they mobilize and release smaller organic molecules used for their growth and metabolic needs (Frąc et al. 2018). They also contribute to the nitrogen cycle, and this component is linked to organic substrates; in forests, almost 90 to 95% of the total soil nitrogen originates from organic matter (Niego et al. 2023). Hence, litter decomposition by saprotrophic fungi increases nitrogen availability in ecosystems. Fungal diversity is essential as a biotic predictor of soil multifunctionality, and fungi are critical to maintaining soil functions (Li et al. 2019). The fungi mineralize the organic nitrogenous components, which can be attributed to the enzymatic secretion profile that depends on the fungus species. It has been reported that the fungal species that form rhizomorphs (Cortinarius, Suillus and Rhizopogon) secrete high levels of nitrogenous compounds and enzymes that degrade cellulose (N-acetylglucosaminidase, β-glucuronidase). Therefore, they are usually abundant in soils with limited nutrients (Leski et al. 2010), and fungi with short/contact hyphae (Russula and Tomentella) usually secrete a large number of enzymes that degrade lignin (phenol-oxidase, primarily laccase). Thus, they easily access and assimilate inorganic nutrients (Ning et al. 2020). Wild fungi are also culturally significant. Although the vast majority of these fungi cannot be cultivated yet (studies are ongoing so that the cultivation can take place), they are essential fungi, either as a source of food with nutritional properties of quality and economic potential because the communities have an economic income with the sale of what they collect (Hall et al. 2003; Boa 2004).

Economic Importance of Wild Edible Mushrooms

Wild mushrooms are a significant forest, food, and economic resource, mainly for rural communities in several countries worldwide (Boa 2004). Witte and Maschwitz (2008) indicated that fungi probably developed the fruiting body at the same time as the evolution of omnivores because some animal species are strictly mycophagous. Since ancient times, man has been interested in mushrooms; the Egyptians (for 4,600 years) believed that the mushroom was the plant of immortality (El Sheikha and Hu 2018) and a gift from the god Osiris; therefore, they decreed that mushrooms were food for royalty only. The Greeks believed that consuming mushrooms gave warriors strength in battle; the Romans called them “food of the gods”, believing they emerged because of lightning strikes from Jupiter (Manzi et al. 1999; Arora and Shepard 2008).

The world trade of mushrooms in 2017 exceeded 1,230,000 tons as fresh or processed products (Pérez-Moreno et al. 2021). Among the commercially essential mushrooms is the Amanita sect. caesarea, Morchella spp., Lactarius sect. deliciosus, and Ramaria spp. For Boletus edulis (porcini) and related species, they are necessary for export (fresh, dried, or in brine); 50,000 tons of Boletus are harvested and sold annually in the national and international market. A Finnish company harvested 1,100 tons of mushrooms mainly Boletus in one year, with a turnover of 7.4 million USD (Cai et al. 2011). Russula griseocarnosa species is a valued species in China. This mushroom is believed to be used for the health of pregnant women, and the price of dried specimens is more than 800 Chinese yuan/kg (approximately $130/kg) (Comandini and Rinaldi 2020).

It has been indicated that there will be an annual growth rate of close to 6% in the intra-industrial trade indexes of edible wild mushrooms in different countries; apparently, the capacity to produce said resource is static, and if changes occur, they tend to decrease. In all countries, the following occurs, including global environmental problems such as deforestation, biodiversity loss, illegal trade, and climate change (de Frutos 2020). Therefore, it is crucial to promote the management of non-timber resources for conservation purposes to maintain ecosystems and, at the same time, improve and guarantee food security, environmentally friendly rural development (work and food), and preserve traditional knowledge (Pérez-Moreno et al. 2021).

The Edibility of Wild Fungi

Mushroom is a high protein content food that is often praised and valued because of its characteristic texture and flavor. It is estimated that there are approximately 2300 species of edible and medicinal wild fungi worldwide (Islam et al. 2019; Martínez-Medina et al. 2021). Peintner et al. (2013) mentioned that in European countries, there are approximately 268 species of wild mushrooms of commercial importance. Mexico is considered the wealthy second country in mushroom culture (Pérez-Moreno et al. 2020), with 371 edible mushroom species distributed among 99 genera (Garibay-Orijel et al. 2014). However, this number could be as high as 450 species by fully integrating traditional knowledge of edible mushrooms (Pérez-Moreno et al. 2020). China is the country with the largest number of edible fungi. Dai et al. (2010) reported 966 taxa (936 species, 23 varieties, three subspecies, and four forms) of edible mushrooms, while Wu et al. (2019) indicated 1662 taxa, of which 1020 are edible, and 692 are medicinal. Li et al. (2021a) conducted a review in this regard and stated that there are 2,006 edible species; the highest number of edible mushroom species was recorded in Asia (1493), followed by Europe (629), North America (487), Africa (351), South America (204), Central America (100), and Oceania (19). Approximately 614 species of edible mushrooms are found on two or more continents.

The interest in edible mushrooms has increased due to the search for foods rich in nutrients and beneficial health effects and providing income alternatives for rural communities (Pilz and Molina 2002). Because of the commercial importance of wild species, such as the matsutake (Tricholoma spp.) and Lactarius spp. (L. deliciosus, L. hatsudake, L. volemus, L. vividus, and L. hygrophoroides), morels (Morchella spp.) and boletus (Boletus spp.), among others, in certain countries can provide a significant economic income for collectors (Boa 2004; De-Román and Boa 2006). It is not yet known how the edible species were identified, and it is suggested that it was by trial and error, considering appearance characteristics (smell, colour, texture, etc.), testing small quantities (taste), and recording any adverse reactions (Li et al. 2021a).

There are several species of mushrooms with no nutritional or inedible value; this denomination is specific to the geographical area because, in several places, edible mushrooms are known only by their generic name, which is a guide to the traditional knowledge of consumption in each region (local practices and preferences). It should be taken into account that with certain species of mushrooms, there is no problem, as there is with Cantharellus species, where several species are consumed (although not all of them have a pleasant flavor). However, for the group of the genus Amanita, it is not possible, because this group presents not only edible species (A. caesarea), but toxic (A. pantherina), deadly (A. verna), and edible post treatment (A. muscaria) (Boa 2004). Approximately 183 mushroom species were reported to require treatment before consumption (Li et al. 2021a) because some mushroom species contain toxins when raw and require treatment (tissue softening and detoxification) before consumption (Niksic et al. 2016). Cooking and pre-treatments help to destroy and eliminate toxic compounds from raw mushrooms, as Rubel and Arora (2008) reported that parboiling is a safe detoxification method for Amanita muscaria.

However, some species of fungus are considered edible in some areas but not in other regions, as in the case of Gyromitra spp., which are edible mushrooms in Finland, Russia, Poland, Lithuania, Estonia, and Sweden, where the product is sold in cans under the brand name Fammarps. The bonnet mushroom (G. esculenta) is highly appreciated. It is considered an exquisite snack after being carefully cooked (Boa 2004; Hall et al. 2007; Li et al. 2021a). Also in southern Chile Gyromitra sp. is considered a meat substitute after treatment, which involves several steps of washing, rinsing, heating, and dehydration (Barreau et al. 2016). However, in some countries (Italy, Spain, and the USA), G. esculenta is not edible (false morels). In this regard, Leathem and Dorran (2007) indicated that 27 poisonings by G. esculenta have been reported; none were fatal, but there was liver damage (33%) and kidney failure (11%). Poisonings were more common in the eastern USA, whereas west of the Rocky Mountains poisonings were rare. Hence, growth conditions (biotic and abiotic factors) are essential. Additionally, the edible species of the Boletus are not consumed in Tanzania; however, in other places, they are widely consumed (China, Italy) and even exported (Boa 2004). The Armillaria mellea is an edible and medicinal mushroom (honey fungus). It has been reported as a saprophytic, pathogenic, and mycorrhizal fungus, and it grows wild on live and dead trees. Young fruiting bodies are considered edible when fully cooked, but there have been cases of allergy to this fungus; therefore, great care must be taken when preparing and consuming it (Sośnicka et al. 2018). In general, few mushrooms are eaten raw, but it should be recommended that the specimens be cooked and/or treated before consumption (Li et al. 2021a).

Fig. 1. Mushroom molecules with antioxidant activity and biological activity

It has been reported that wild mushrooms may have higher concentrations of secondary metabolites than cultivated mushrooms, which could result from the selection of mushroom cultivation that flavour yield without considering the quality of secondary metabolites. This is probably because the substrates used may not provide the necessary nutrients, and the climatic and environmental influence may contribute to these differences by providing optimal growth conditions (pH, light, humidity, temperature, etc.), where the natural environmental stress influences the production of secondary metabolites (Mwangi et al. 2022). Edible wild mushrooms have had great importance within the population, either as food, medicine, or both; they are essential for the survival and economy of ethnic groups and present components that have attributions to health (Lakhanpal and Rana 2005; Chang 2006).

Most mushrooms are rich in non-starch polysaccharides, beta-glucans, dietary fibre, protein, ergosterol, statins, minerals, etc. (Fig. 1), which have antioxidant activity (Novaković et al. 2020). Pharmacological studies of fungi have shown that Basidiomycete and Ascomycete are immense sources of biologically active molecules. Still, less than 10% of all species have been described, and even fewer have been analyzed for their therapeutic effects (Smith et al. 2015). Despite this lack of general characterization of active compounds, edible fungi are frequently recognized as nutraceuticals or functional foods because, in addition to their nutritional value, they often have medicinal benefits (Rasalanavho et al. 2020), as is the case with phenolic compounds that have been attributed to antitumor, hypoglycemic, cytotoxic, and antihyperlipidemic activity, among others.

Phenolic Compounds in Edible Mushrooms

Two groups of phenolic acids are distinguished: derivatives of benzoic acid and cinnamic acid. Several authors have indicated that the leading phenolic group in fungi is phenolic acids, to which biological activities have been attributed (Muszyńska et al. 2013b; Taofiq et al. 2015; Nowacka-Jechalke et al. 2018). Such activity has been confirmed for certain phenolic compounds, as in the case of Macrolepiota procera, for which the researchers identified the molecules involved in the anti-inflammatory activity and determined the presence of cinnamic, ρ-coumaric, and ρ-hydroxybenzoic acids (Taofiq et al. 2015). For Calocybe, the in vitro activity of antityrosinase was correlated with the presence of six phenolic acids (gallic, homogentisic, protocatechuic, chlorogenic, caffeic, and ferulic) present in acetone, methanol, and hot water extracts (Alam et al. 2019). In another study with antibacterial activity against Escherichia coli, Pseudomonas aeruginosa, Klebsiella pneumoniae, Staphylococcus aureus, S. epidermidis, and Bacillus subtilis, the methanolic crude extract presented several compounds, including phenolic acids (Datta et al. 2020). Ghosh et al. (2020) indicated that an ethyl acetate extract of the fruiting body of C. indica inhibited the formation of colonies, cell migration, and cell proliferation of HeLa and CaSki (cervical cancer cell lines); the analysis of the extract showed the presence of phenolic compounds, flavonoids, and ascorbic acid.

Erbiai et al. (2021) showed that there was a quantitative difference between samples of A. mellea from northern Morocco and Portugal; in the species of fungi from the latter site, cinnamic acid (155.2 μg/g dw), protocatechuic acid (43.90 μg/g dw), and ρ-hydroxybenzoic acid (43.85 μg/g dw), and for A. mellea from northern Morocco vanillic acid (198.4 μg/g dw) was found, followed by cinnamic (100.6 μg/g), proto-catechuic (48.34 μg/dw), and gallic acids (32.24 μg/g dw). Another important edible mushroom Sparassis crispa is consumed in Japan, and to date, it is considered a safe therapy for chronic diseases and cancer (Kimura et al. 2013). Kim et al. (2008) reported that the methanol extract from the fruiting body of S. crispa from Korea, commonly known as cauliflower mushroom because of the shape of the above-ground basidiomes, presented 764 μg/g phenolic compounds and 15 phenolic compounds: gallic acid, pyrogallol, 5-sulfosalicylic acid, protocatechuic acid, ρ-hydroxybenzoic acid, vanillic acid; caffeic acid, syringic acid, ρ-coumaric acid, veratric acid, benzoic acid, resveratrol, quercetin, naringenin, and kaempferol. However, Sułkowska-Ziaja et al. (2015) indicate that an extract using HCl (2M) and ethyl acetate presented seven phenolic compounds (gallic acid, ρ-hydroxybenzoic acid, caffeic acid, ρ-coumarin acid, protocatechuic acid, and syringic acid) and 85.65 mg/100 g of total phenols in fruiting bodies of a different strain of S. crispa obtained from northern Poland. Another review reports six phenolic compounds for S. crispa in aqueous and methanol extracts (protocatechuic acid, ρ-hydroxybenzoic acid, syringic acid, ρ-coumaric acid, gallic acid, pyrogallol, and quercetin); the fruiting bodies were obtained from India, Korea, and Poland (Quintero-Cabello et al. 2021). There is a difference in the content and type of phenolic compounds reported, hence it is also very important to consider the origin and processing of samples, as depending on the growth condition (biotic and abiotic factors), there is a difference in the production of metabolites.

Several solvents have been used, ranging from polar to non-polar (water, acidic water, ethanol, methanol, acetone, ethyl acetate, chloroform, etc.). Solvents perform a selective extraction of specific molecules, which could improve the antioxidant activity, indicating that in some cases, increasing the polarity of the solvent results in higher extraction performance of phenolic compounds (Petrović et al. 2014) and presents more significant bioactivity (Truong et al. 2019). Still, obtaining bioactive compounds (phenolic and antioxidants) depends on multiple factors, and the solvent is one of them. In this regard, Fogarasi et al. (2021) compared the antioxidant activity and phenolic compounds obtained from the powder of fruiting bodies with different solvents. In general, the order of the content of phenolic compounds (in decreasing order) extracted with each solvent was water, hydroalcoholic, hexane, and diethyl ether. Seventeen phenolic compounds were determined in water and hydroalcoholic extracts of Boletus edulis, while only five were found in the hexane and ethanol extracts. For Cantharellus cibarius, there were 14 in water, four in ethanol, and only two in hexane. The genus Melanoleuca has approximately 50 species worldwide (Ainsworth 2008); the M. cognata and M. stridula (consumed in Turkey) reported six phenolic compounds were quantified in ethyl acetate extracts, methanol, and water (benzoic acid, ρ-coumaric acid, ρ-hydroxybenzoic acid, protocatechuic acid, syringic acid, and trans-cinnamic acid); the syringic acid was the main phenolic in both species, followed by benzoic acid (34.1 and 32.2 μg/g dw, respectively). There was no difference in the presence of phenolic compounds depending on the solvent, but there was a higher content of phenolic compounds and antioxidant activity in water extracts (Bahadori et al. 2019).

Bioactive molecules can lose their activity due to the extraction processes because they can be eluted and destroyed. One of the crucial factors is the temperature. When they are taken out at high temperatures, it can cause the destruction or loss of active compounds that are vulnerable to heat, but when doing the extraction at low temperatures it could be that these compounds are not correctly extracted. Liang et al. (2010) reported that the ethanol and hot water extracts of mycelium and S. crispa culture broth identified five compounds in the ethanol extract (ascorbic acid, β-carotene, α-tocopherol, and gamma-tocopherol) and only two in the hot water extract (ascorbic acid and α-tocopherol) in the mycelium. However, in the culture broth with ethanol, there were two compounds (ascorbic acid and α-tocopherol); in hot water, only ascorbic acid was detected. Both extracts had antioxidant activity and reducing power, but high temperature decreased the content of phenolic compounds. Lee et al. (2016) reported that high temperature favoured the S. crispa mycelium extract when exposed to 95 °C. It presented 30.3 mg GAE/g of polyphenols and 2.65 mg QE/g of flavonoids, compared to the 60 °C extract that had 26.8 mg GAE/ g and 2.02 mg QE/g. For the extract from the fruiting body, it was 25.7 mg GAE/g of polyphenols and 1.5 mg QE/g flavonoids at 95 °C. At 60 °C, it was 19 mg GAE/g and 0.54 mg QE/g, respectively. The mycelium contains many components, and the elution of the elements was better when extracted at high temperatures.

It has been documented that the processing of samples affects polyphenol content. This is because physical processes, such as crushing, could cause oxidative degradation of polyphenols by cell breakdown, cytoplasmic oxidase enzymes, and phenolic substrates present in vacuoles (Manach et al. 2004). There are several studies on the content of polyphenols in edible fungi (Table 1). Still, it is difficult to compare them due to the diversity of the research material (geographical area, cellular stage, the composition of the procurement site, etc.), growth factors, drying method, solvent type, extraction process, analysis, and expression of the results.

Table 1. Phenolic Compounds of Edible Mushrooms