Oudemansiella (Physalacriaceae) mushrooms: A status review on the distribution, cultivation, composition and bioactivity profile

Mushrooms are edible or poisonous, epigeous or hypogeous, Basidiomycetous or Ascomycetous macrofungi. They can be grouped into an edible, medicinal, poisonous, and miscellaneous groups including under-utilized and undiscovered species. Mushrooms act as saprophytic, parasitic, and symbiotic (mycorrhiza), making them essential in the decomposition of massive forest litters, cycling of nutrients and maintenance of ecological balance^[1]. As food, mushrooms are very nutritious and highly medicinal. They are a rich source of proteins, carbohydrates, dietary fiber, ergosterol, minerals such as calcium, copper, iron, magnesium, manganese, phosphorus, potassium, selenium, and zinc, and vitamins like thiamin, riboflavin, niacin, pantothenic acid and pyridoxine^[2]. Bioactive proteins such as lectins and enzymes immunomodulatory fungal proteins have been widely reported to exhibit antibacterial, antifungal, antiviral, antitumor and immunoenhancing properties^[3]. Phenolic compounds (quercetin, catechin, myricetin, pyrogallol and caffeic acid), carotenoids, ergosterols, tocopherols, ascorbic acid, terpenes and polysaccharides present in the mycelia and fruiting bodies of edible mushrooms showed antioxidant, anti-inflammatory and anticancer activities^[4]. Active ingredients of mushroom, such as polysaccharides, terpenoids, proteins, fatty acids, nucleotides, sterols, steroids and vitamins showed antidiabetic, anti-oxidant, anticancer, anti-atherosclerotic, anti-inflammatory, antimicrobial, antiangiogenic, anti-arthritic, anti-herpetic, anti-nociceptive, anti-androgenic, antiaging, antiulcer, anti-fibrotic, anti-osteoporotic, hepatoprotective, hypolipidemic, chemopreventive, analgesic, immunomodulatory and estrogenic activities^[5].

Oudemansiella (Physalacriaceae, Agaricomycetes, Basidiomycota) are widely distributed in tropical and subtropical regions and are known as saprophytic fungi that grow in decaying leaves and wood of trees^[6]. They are characterized morphologically by their ixotrichodermpileipellis, which are made of filamentous hyphae commonly intermixed with chains of inflated cells^[7]. In addition, its pileus is often dry to viscid, with white to off-white lamellae and a central stipe lacking a persistent />annulus^[7,8]. Traditionally, Oudemansiella has been a broad-based genus that includes Xerula Maire and Mucidula Pat. species^[9]. However, Baekhout & Bass^[10] claimed that Oudemansiella and Xerula are two distinct genera based on morphological differences such as basidiocarp development, pseudorrhiza, spore size, and shape, among others. Meanwhile, Alberti et al.^[8] argued in their review that many researchers classified Oudemansiella, Xerula, and Mucidula to be distinct genera. Niego et al.^[7] supported this taxonomy and mentioned that the basidiomata of Oudemansiella vary from those of Mucidula in microscopical parameters by lacking a persistent annulus on the stipe and that the former genus is exclusively found in tropical regions.

The interest on the nutritional and pharmacological properties of wild mushrooms for functional food and alternative drug development is continuously increasing worldwide. The cultivation potentials and the biological activities of Oudemansiella species have been explored^[11−14]. Herein, we comprehensively reviewed the status in terms of the global records, distribution, cultivation, bioactive compositions and bioactivities of Oudemansiella species in order to provide benchmark data for their conservation and maximum utilization.

The distribution of the mushroom is determined by both nutritional and physical factors such as temperature, humidity, substrate composition, elevation, and climatic conditions^[1]. Members of the Physalacriaceae mushrooms thrive in a wide range of temperatures, as evidenced by records from both tropical and subtropical regions^[6,8,15]. In this review, a total of 25 species of Oudemansiella were recorded viz. O. americana, O. andina, O. australis, O. bii, O. canarii, O. cephalocystidiata, O. crassifolia, O. cubensis, O. echinosperma, O. ephippium, O. exannulata, O. fanjinshanensis, O. globospora, O. gloriosa, O. haasiana, O. indica, O. latilamellata, O. melanotricha, O. munnarensis, O. orinocensis, O. platensis, O. reticulata, O. rhodophylla, O. submucida, O. yunnanensis (Table 1). The Oudemansiella species were reported in 31 countries in Asia, North and South America, Australia, Africa, and Europe. Among species, O. canarii was found to be the most widely distributed (14 countries), followed by O. platensis (nine countries), O. cubensis (seven countries), O. melanotricha (five countries), and O. submucida and O. australis (three countries) (Fig. 1). On the other hand, China had the greatest number of reported species of Oudemansiella (eight species), followed by Brazil and Australia (five species each), Argentina (four species), and India, Thailand, and Costa Rica (three species each) (Fig. 2). The geographic distribution of the most widely distributed Oudemansiella species in the world is shown in Fig. 3.

Figure 1. 

Most widely distributed Oudemansiella species worldwide.

Figure 2. 

Top countries with the greatest number of reported Oudemansiella species.

Figure 3. 

Geographical distribution of Oudemansiella species worldwide.

Compared to the recent review of Niego et al.^[7], they only recorded a total of 14 species of Oudemansiella, which includes O. alphitophylla, O. bii, O. canarii, O. crassifolia, O. exannulata, O. fanjingshanensis, O. gloriosa, O. latilamellata, O. platensis var. orinocensi, O. rhodophylla, O. reticulata, O. submucida, O. turbinospora, and O. yunnanensis. This is significantly lower than the recorded number of species reported in this review. Additionally, based on Species Fungorum, two of the Oudemansiella mushrooms mentioned in their review, the O. platensis var. orinocensi and O. alphitophylla, were assigned to another species (Oudemansiella orinocensis) and genera (Chamaemyces alphitophyllus), respectively. Therefore, it is safe to conclude that the present review provides a comprehensive checklist and the distribution of Oudemansiella species worldwide.

The climatic condition of the geographic origin of Oudemansiellla species is one of the major factors that affects their distribution and diversity. Based on the data gathered, Oudemansiella species could grow in a wide range of temperatures, from tropical to temperate conditions of different countries. This supports the claims by Niego et al.^[7] who reported that Oudemansiella can be found worldwide, primarily in tropical and subtropical regions. Given that the majority of these mushrooms are wood-rotting and leaf litter macrofungi, another possible reason for the wide distribution of the Oudemansiella is the rich vegetation in the rainforest of the cited countries. Rainforests offer a great substratum that is suitable as a growing medium for wild mushrooms like Oudemansiella. Furthermore, in a recent study by Lopez & Undan^[19], they successfully identified the first species of Oudemansiella australis in the Philippines using a molecular approach, wherein its last records were found in Papua New Guinea and Australia in 2001. Hence, continuous efforts on the myco-expedition and mycodiversity assessment in the wild by mycologists, mycotaxonomists and researchers are imperative to reveal more Oudemansiella species that remain to be explored.

Altogether, the climatic conditions of geographical origin and vegetation have significant impact on the diversity and distribution of Oudemansiella. The recent findings on the new records of Oudemansiella species in different countries^{[7,8,19,28,32,34]} strongly indicate that there are still more Oudemansiella species in the wild waiting to be discovered and harnessing of their various promising potential.

In the present review, the different technologies for the cultivation of Oudemansiella species were also gathered (Table 2). It can be seen that only two Oudemansiella species were evaluated for their fruiting body cultivation, and Oudemansiella canarii was the most commonly evaluated for cultivation. Several agro-industrial wastes such as sugarcane bagasse, eucalyptus sawdust, cotton seed hull, corncob, sawdust, and rice straw were used as basal substrates in the production of Oudemansiella fruiting body^{[12,20,21,56]}. In terms of the biological efficiency, O. canarii showed significantly varied biological efficiencies depending on the substrate used and most likely on the origin of the mushroom strains used in the individual study.

Silveira Ruegger et al.^[20] used sugarcane bagasse and eucalyptus sawdust supplemented with wheat bran for the fruiting body cultivation of O. canarii strain CCB179. They found out that growing O. canarii in sugarcane bagasse incorporated with 50 g wheat bran, incubated at 25 °C, resulted in higher biological efficiency (55.66%), productivity (4.47%), and compost consumption (38.78%). Fruiting bags containing eucalyptus sawdust supplemented with wheat bran recorded 19.51% only. Xu et al.^[21] cultivated O. canarii fruiting bodies using lignocellulosic wastes such as cotton seed hull, sawdust, corncob, and their combinations supplemented with 18% wheat bran and 2% lime incubated at 25 °C and 70% relative humidity in dark condition. Substrate with 80% cotton seed hull, 18% wheat bran and 2% lime produced the greatest yield of 7,955.1 g and recorded the highest biological efficiency of 113.64%. However, this was not significantly different to the yield and biological efficiency of mushroom cultivated in substrate containing 40% cotton seed hull, 40% corncob, 18% wheat bran and 2% lime.

Dulay & Damaso^[12] successfully domesticated and cultivated a wild strain of O. canarii BIL 9137 from Lingap Kalikasan of Central Luzon State University, Science City of Munoz, Nueva Ecija, Philippines. They also reported that malt extract agar (64.83 mm) and potato broth sucrose agar (84.17 mm) showed the widest mycelial diameter with very thick mycelia. Sorghum seeds and cracked corn were found to be most suitable grain spawn materials, which showed the lowest incubation period of 11.33 d. Rice straw and sawdust at 8:2 ratio was identified as the best substrate formulation for the fruiting body cultivation of O. canarii. The mycelia and fruiting bodies of O. canarii grown in their most suitable medium are shown in Fig. 4. The stages of fruiting body development of O. canarii from primordial initiation to fruiting body maturation were also documented.

Figure 4. 

(a) Mycelia and (b) fruiting bodies of O. canarii^[12].

In comparison with other Physalacriaceae species such as Flammulina velutipes, Harith et al.^[58] also utilized agro-industrial waste such as rubber wood sawdust, paddy straw, palm empty fruit bunches, and palm-pressed fiber supplemented with spent brewer’s yeast and rice bran as nitrogen sources at the ratios of 3:1, 1:1, and 1:3 for fruiting body cultivation of F. velutipes. Similarly, agro-industrial waste shows excellent substrate material resulting in excellent biological efficiency (BE). Based on their findings, the best substrates were paddy straw + palm empty fruit bunches (25:75 substrate formulation) with 185.09% BE, paddy straw + palm-pressed fiber (50:50) with 150.89% BE, and palm-pressed fiber (100) with 129.06% BE.

Given the limited studies on the cultivation of Oudemansiella species, this unlocks important research topics and efforts on the optimization studies, enriched cultivation, and submerged cultivation, which are necessary to develop more production technologies for this group of mushrooms in order to ensure conservation and sustainability.

Mushrooms are widely utilized as a source of food and/or traditional medicine worldwide. Edible mushrooms are an excellent source of nutritious and unique umami-tasting food. They are rich in carbohydrates, proteins, fibers, vitamins, minerals, and low-fat content^[59,60]. The dry matter of mushrooms, in general, contains 50%-65% carbohydrate, 19%−35% protein, and 2%−6% fat^[61]. The approximate composition of O. canarii and O. submucida and the most commonly cultivated edible mushrooms in the world are summarized in Table 3. Zhou et al.^[53] revealed that O. submucida contains 27.41% total carbohydrate, 3.95% fiber, 14.70% protein, and 7.10% fat. The carbohydrate compositions include arabitol (15.95%), mannitol (2.90%), glucose (0.97%), soluble polysaccharides (4.00%), and fiber (3.95%). This mushroom also contains 15 amino acids including alanine, arginine, aspartic acid, glutamic acid, glycine, histidine, isoleucine, leucine, lysine, phenylalanine, proline, serine, threonine, tyrosine, and valine with a total of 18.09%. On the other hand, O. canarii contains 33.39% carbohydrates, 16.65% protein, 33.52% fiber, 1.64% fats, 8.13% ash, essential and non-essential amino acids^[21]. Accordingly, the amount of chemical compositions of mushroom varies depending on the species. Carbohydrates are the major components of the six mushrooms (Table 3). The major carbohydrate content of mushrooms include glucose, fructose, sucrose, maltose, arabinose, rhamnose, mannitol, trehalose, and xylose^[61,62]. Lipids are the lowest composition of mushrooms. However, the major fatty acid content of mushrooms include linoleic acid, oleic acid, palmitic acid, and stearic acid^[63]. Linoleic acid has been reported to exhibit anti-obesogenic, anti-carcinogenic, and anti-atherosclerotic properties^[64]. Moreover, tocopherol is known as an effective antioxidant^[65], whereas ergosterol is known as a precursor of vitamin D2^[66].

Edible mushrooms have been exploited for a very long time as natural alternative remedies for various diseases. The therapeutic values and medicinal properties of edible mushrooms have found to stem from numerous biologically active compounds or metabolites^[70]. The crude extracts and bioactive compounds and the corresponding biological activities of Oudemansiella species are summarized in Table 4. Among Oudemansiella species, only two species namely, O. canarii and O. melanotricha, have been evaluated for biological properties, which are reported in six separate studies. Crude extracts of O. canarii extracted using ethyl acetate, ethanol and methanol as extracting solvents have been found to exhibit antifungal, antioxidant and cytotoxic activities and inhibit trypanothione reductase (TryR)^{[11,13,14,71]}. Moreover, bioactive compounds such as oudemansin A, dihydroxerulin, xerulinic acid, oudemansin B and strobilurin C have been successfully isolated from Oudemansiella species, and have been shown to display antimicrobial activities^[11,72,73]. The chemical structures of the five mentioned bioactive compounds of Oudemansiella obtained from Pubchem (https://pubchem.ncbi.nlm.nih.gov/) are presented in Fig. 5. Accordingly, Oudemansiella species could be valuable natural resources of extracts and bioactive compounds that possess pharmacological and nutraceutical properties.

Figure 5. 

Chemical structures of bioactive compounds of Oudemansiella (National Center for Biotechnology Information (2022). PubChem Compound Summary for CID 6438712 oudemansin A and B, 131569 dihydroxerulin, 6439346 xerulinic acid 76968370, and strobilurin C. Retrieved December 14, 2022, from https://pubchem.ncbi.nlm.nih.gov/.

Dulay et al.^[14] studied the cytotoxic activities of ethanol extract of wild fruiting bodies of O. canarii against nine hematologic malignant cells and the underlying molecular mechanisms. They found out that O. canarii extract exhibited cytotoxicity with IC₅₀ values of 26.8–66.0 ppm and inhibited cell proliferation by 57.3%–72.5% in all the cancer cell lines used. After 48 h of exposure, extract-treated cancer cells displayed 68.2%–82.5% Annexin-V positive cells, and showed a significant increase of cells in the sub G0/G1 phase from 5.3%–22.5% (control group) to 59.8%–87.5%. The presence of O. canarii extract displayed an increase in the production of ROS by 4.32-fold in KBU, 2.96-fold in MOLM13, 7.42-fold in J45.01, 3.73-fold in U937, 7.40-fold in RPMI 8226, and 5.22-fold in MM.1R, and showed a significant increase in the monomer/aggregate ratio between 0.64 and 5.95, which strongly suggest that O. canarii extract can induce mitochondrial dysfunction. Activation of apoptosis-related markers and stress-activated protein kinase (SAPK/JNK) signaling pathway is one of the potential mechanisms of the cytotoxicity of O. canarii extract against leukemia, lymphoma, and myeloma cells. The bioactive metabolites of O. canarii have not yet been identified in their study and it warrants further investigation.

Antioxidants are one of the most important biological/pharmacological properties of O. canarii^[13]. Most studies have also reported that the bioactive compounds isolated from Oudemansiella species have potent antimicrobial activity^[72]. Accordingly, studies on the functionality profile of Oudemansiella species are very limited. It is therefore of urgent need to popularize this mushroom group through commercial cultivation for industrial application, and increase the number of researchers who will be working on this aspect. More advanced work on bioactivity profiling, product development, and commercialization of the developed functional foods, dietary supplements, and alternative drugs are imperative.

The geographical distribution, cultivation, composition and bioactivity of Oudemansiella species were highlighted in this review. In particular, this paper provides the global distribution of 25 Oudemansiella species, cultivation potential with reference to their substrate requirements for fruiting body production, proximate compositions and isolated bioactive com/>pounds, and biological properties of Oudemansiella. It is also revealed that only two species (O. canarii and O. melanotricha) have been thoroughly studied for bioactivity evaluation, and the bioactivity is limited to anticancer, antifungal, antioxidant, cytotoxicity, and antibacterial activities. Furthermore, the industrial applicability of Oudemensiella has not yet been explored.

Based on the information gathered in this study, the following should be considered for future research; (a) wider scope of assessments of the world's mycodiversity particularly those countries with suitable environments for the growth of Oudemansiella, (b) accurate identification and characterization of other Oudemansiella species through taxonomic and phylogenetic analysis using new molecular techniques to identify new Oudemansiella species, (c) mycelial growth optimization, nutrient source optimization, and submerged cultivation in order to establish the full potential of this mushroom group for cultivation and to popularize their utilization in various industrial applications, (d) evaluation of more functional activities in various biological systems or models and establish their mechanism of action, (e) elucidation, characterization, and identification of novel bioactive compounds responsible for the observed bioactivities, and (f) exploration of Oudemansiella mushrooms for the development of functional foods, dietary supplements, and pharmaceutical drugs in order to fully realize their importance for the benefits of mankind.