Status review of the distribution, biological compounds, and bioactivity of Coprinellus (inky cap mushroom)

Psathyrellaceae Vilgalys, Montecalvo & Redhead mushrooms are characterized by having a deliquescent fruiting body that has a special autodigestive phase of ontogeny on which the maturing fruiting body undergoes extensive cell autolysis that involves all the tissues of the cap and becomes a blackish inky fluid when mixed with a blackish mass of spores^[1]. According to Sharp^[2] and Nagy et al.^[1], Psathyrellaceae mushrooms are morphologically characterized by their small to medium-sized, dark-spored, delicate fruiting bodies, which frequently have soft, delicate stems and caps. In an earlier classification, Psathyrellaceae, formerly known as Coprinaceae, are divided into two large genera: the autodigesting species of Coprinus Pers. and the non-autodigesting species of Psathyrella, respectively^[1]. These mushrooms are widely distributed in both tropical and temperate countries, which thrive in different types of substrates such as soils, leaf litter, dead branches, and ruminant dung, among others^[3−20].

The Coprinellus mushrooms, one of the genera belonging to Psathyrellaceae, were derived from Coprinus (Pseudocoprinus Kühner), and were introduced to accommodate partially deliquescent species (such as Coprinellus disseminatus) and are now recognized as one of the established genera of Psathyrellaceae with over 71 species recorded based on the mycological data of the Species Fungorum^[21]. In terms of its morphology, Coprinellus species are divided into three large clades, the Setulusi, Micacei, and Domestici clades, based on the existence of cap pileocystidia and the morphology of its veil^[13,22]. Although these groupings tend to reflect morphological characteristics, molecular studies have demonstrated some phylogenetic inconsistencies, particularly in the distribution of setulose within clades^[23]. In addition, Coprinellus is one of the coprinoid or inky caps fungi that exhibit distinctive features, including the dark pigmented basidiospores, occurrence of pseudoparaphyses in the hymenium, deliquescent lamellae, and sequential basidial development^[24]. Similar to all other coprinoid genera, Coprinellus species can be distinguished from typical agarics by their gills, which liquefy as the mushroom matures^[22]. Moreover, Coprinellus immature gills are not pinkish, with either present or absent veil, deliquescent or non-deliquescent cap during sporulation, and the pileipellis consists of hymeniderm or cystoderm of globose to piriform cells^[25]. Ecologically, Coprinellus is characterized as a saprophytic fungus that grows in nutrient-rich substrates, including dead trees, branches, leaf litter, grassy debris, bare soil, and ruminant dung^[26].

Furthermore, various studies have already classified taxonomically the different species of Coprinellus, particularly the newly recorded species from diverse countries. In the study of Gomes & Wartchow^[27], they reported the taxonomy of the new species Coprinellus arenicola isolated from Paraíba, Brazil, based on its holotype, basidiomata, pileus, lamellae, stipe, basal mycelium, basidiospores, basidia, cheilocystidia, pileipellis, stipitipellis, elements of veil on pileus, etymology, habitat, and distribution. Accordingly, C. arenicola is a newly described species of small, subgregarious basidiomycete fungi characterized by a buff to pale beige, plicate-pectinate pileus, adnexed grayish to black lamellae, a smooth, white, hollow stipe, an absent annulus, heart-shaped to triangular basidiospores, and habitat specificity to sandy soils in Paraíba, Brazil. Similarly, Coprinellus ovatus from Pakistan is characterized as a small, caespitose fungus with an orange-yellow, fibrillose, plicate pileus, free brownish-black lamellae, a yellowish-brown radicating stipe, mitriform to amygdaliform basidiospores, utriform cheilocystidia, and grows among broadleaf trees^[22]. Overall, different species of Coprinellus share similar features such as deliquescent lamellae, small basidiomata, and saprophytic nutrition since they all belong to the same family, Psathyrellaceae, but can be morphologically distinguished from one another based on the differences in color of the lamella, stipe, structure of basidiospore, presence or absence of cheilocystidia, color, and structure of pileus, among others.

Furthermore, Coprinellus mushrooms are widely documented and studied, with Europe being among the top continents with the most Coprinellus mushrooms recorded^{[6,8,13,16,18,23,24,28−49]}. Aside from species identification, the different bioactivities of the genus Coprinellus have also been elucidated, including antifungal^[50], anticholinesterase^[51], and antioxidant^[46] activities. Moreover, the co-culturing of C. radians and C. disseminatus stimulates seed germination in Cremastra appendiculata^[52,53].

In addition to their bioactivities, novel bioactive compounds were also screened in Coprinellus mushrooms. For instance, Tešanović et al.^[46] extracted different phenolic compounds such as flavones, flavonols, flavanones, flavanols, bioflavonoids, isoflavonoids, hydroxybenzoic acids, hydroxycinnamic acids, coumarins, cyclohexanecarboxylic acids, and chlorogenic acids in the hot water extract of C. truncorum. Meanwhile, in the qualitative analysis of the fatty acid composition of Coprinellus curtus, C. disseminatus, C. domesticus, Coprinellus ellissi, C. micaceus, and C. radians mycelia, both unsaturated (linoleic and oleic) and saturated (palmitic, stearic, and myristic) fatty acids were present^[29].

Given the potential of Coprinellus, this review highlights the global distribution, various bioactive compounds, and biological activities of Coprinellus mushrooms, emphasizing their importance in different industries and underscoring the gaps for future studies.

Nutritional and physical factors, including substrates, microclimates, temperature, pH, humidity, and elevation, significantly influence the distribution of mushrooms. Given this environmental sensitivity, the ability of Psathyrellaceae mushrooms to thrive across a wide range of climatic conditions is particularly notable, as evident in their global distribution records^[3−20]. Moreover, Coprinellus mushrooms, belonging to the family Psathyrellaceae, also display broad thermal tolerance, as recorded in both tropical and temperate countries (Fig. 1). In the present review, a total of 67 Coprinellus mushrooms were recorded based on available reports from various studies, including species listing, diversity assessment, biological compound profiling, and bioactivity assessments (Table 1). The Coprinellus mushrooms demonstrated a wide geographical distribution, with the USA, Hungary, Argentina, China, Brazil, and Armenia representing the countries with the most recorded instances of Coprinellus mushrooms (Fig. 2). Notably, particular species of Coprinellus exhibit broad distributions, including Coprinellus disseminatus, Coprinellus micaceus, Coprinellus radians, Coprinellus domesticus, and Coprinellus flocculosus, which are among the top species of Coprinellus that are widely distributed (Fig. 3).

Figure 1. 

Global occurrence patterns of Coprinellus mushrooms, visualized using filled map tools in Microsoft Excel 2019.

Figure 2. 

Countries with the highest reported species diversity of Coprinellus.

Figure 3. 

Coprinellus species with the broadest global occurrence.

The distribution and diversity of Coprinellus species are influenced by the climate of their native regions and the abundant vegetation that provides the necessary nutrients for fungal growth. According to Schafer^[26], Coprinellus mushrooms are saprotrophic fungi that grow on decaying plant material, such as wood, leaves, grass, and animal dung, primarily from ruminants. This ecological versatility enables the widespread distribution of Coprinellus mushrooms, as both temperate and tropical regions offer the requisite substrates, such as decaying organic matter and ruminant dung, ensuring the mushrooms' survival across diverse climates. In addition, efforts in extensive macrofungal identification and domestication play an important role in the abundant records of Coprinellus species, particularly in Europe. Accordingly, approximately 43.87% of the Coprinellus reports are from Europe, with only 29.68%, 24.52%, and 1.94% from Asia, the Americas (encompassing both North America and South America), and Africa, respectively (Fig. 4).

Figure 4. 

Percentage of Coprinellus species recorded across continents.

In comparison with the data from the present review, other studies have also reported different species of Coprinellus. For instance, the study of Doveri^[8] on the occurrence of coprophilous Basidiomycetes and Ascomycetes in Italy recorded a total of 12 species of Coprinellus mushrooms. Meanwhile, the evolutionary and divergence study of Psathyrellaceae of Nagy et al.^[32] utilizes 18 Coprinellus species in Hungary; however, seven of these species, particularly Coprinellus bisporus, Coprinellus callinus, Coprinellus congregatus, Coprinellus hiascens, Coprinellus pellucidus, Coprinellus sassii, and Coprinellus subpurpureus have been reclassified under the genus Ephemerocybe (Ephemerocybe bispora, Ephemerocybe callina, Ephemerocybe congregata, Ephemerocybe hiascens, Ephemerocybe pellucida, Ephemerocybe sassii, and Ephemerocybe subpurpurea, respectively) within the same family, Psathyrellaceae. In addition, 37 Coprinellus species utilize in different studies, specifically Coprinellus allovelus^[9,28], Coprinellus amphithalus^[18], Coprinellus angulatus^{[13,15,18,67,98]}, Coprinellus bisporiger^[9,13], Coprinellus bisporus^[8,13,29,99], Coprinellus brevisetulosus^[8,13,67], Coprinellus callinus^[13,18], Coprinellus canistrii^[100], Coprinellus christianopolitanus^[16], Coprinellus cineropallidus^[13], Coprinellus cinnamomeotinctus^[49], Coprinellus congregatus^[8,34,101], Coprinellus doverii^[8], Coprinellus eurysporus^[13,102], Coprinellus fallax^[21], Coprinellus furocystidiatus^[23], Coprinellus hetersetulosus^[8], Coprinellus heterothrix^[9,34,49], Coprinellus hiascens^[8,13,36,67], Coprinellus marculentus^[8,42,98], Coprinellus minutisporus^[28], Coprinellus mitrinodulisporus^[28], Coprinellus pallidus^[18], Coprinellus pellucidus^[8,13,36,67], Coprinellus plagiosporus^[13], Coprinellus pseudoamphitalus^[28], Coprinellus pseudodisseminatus^[12], Coprinellus radicellus^[9,13,103], Coprinellus sublicola^[18], Coprinellus sassii^[8,13], Coprinellus sclerocystidiosus^[13,18], Coprinellus singularis^[21], Coprinellus subdisseminatus^[42], Coprinellus subimpatiens^{[11,15,18,45,67]}, Coprinellus subpurpureus^[34], Coprinellus uljei^[13], and Coprinellus velatopruinatus^[36] have also been reclassified under genus Ephemerocybe. Moreover, individual records of Coprinellus species, such as Coprinellus arenicola^[27], Coprinellus ovatus^[22], Coprinellus parvulus^[24], and Coprinellus aureogranulatus^[12] have also been reported in different countries. Notably, Hussain et al.^[13] described three new species of Coprinellus in Pakistan (Coprinellus campanulatus, Coprinellus disseminatus-similis, and Coprinellus tenuis) and utilized a total of 25 species of Coprinellus from 97 sequences from the ITS datasets at the National Center for Biotechnology Information (NCBI) website to differentiate these three new species.

Despite these extensive records, taxonomic inconsistencies and outdated classifications persist in the literature. According to Voto^[55], while working on a worldwide key to genera and species of the family Psathyrellaceae, several taxa were noted to have improper status, emphasizing the need to correct invalid species names in publications. Therefore, this present review, in line with the listing from Species Fungorum, provides an updated and corrected distribution of Coprinellus worldwide based on available reports.

Therefore, it is evident that the present review provides the most extensive accounts of Coprinellus species distribution to date. Notably, to the author's knowledge, this is the first comprehensive report on the global distribution of Coprinellus, offering valuable baseline data for future studies on their ecology, cultivation, and potential utilization. Given the widespread occurrence of these mushrooms across diverse climates and substrates, as highlighted in this review, such data are crucial for guiding conservation efforts, bioprospecting, and effective utilization in different industries.

Mushrooms are widely utilized as a source of food and traditional medicine worldwide, as they are known to contain essential nutrients, vitamins, minerals, mycochemicals, and mycocompounds have been shown to be beneficial to human health^[30]. However, the edibility and nutritional benefits of most of the mushrooms were limited due to a lack of research. Therefore, continuous efforts to discover the nutritional composition of mushrooms and their biological compounds enable researchers to harness their beneficial nutrients. Accordingly, mushrooms are known to contain various bioactive compounds that are responsible for their distinct bioactivities. These compounds make mushrooms essential for many industries, including pharmaceutical, nutraceutical, and food industries, among others. According to Kour et al.^[104], a variety of bioactive compounds, such as peptides, polysaccharides, proteins, polysaccharide-protein complexes, phenolic compounds, and terpenoids, have been identified in different types of mushrooms. Meanwhile, in the Philippines, approximately 15.53% of the macrofungal studies focused on elucidating the chemical composition of different mushroom species, particularly their proximate compositions, including protein, fats, moisture, fiber, and carbohydrates, as well as amino acid and fatty acid composition, and various mychochemicals^[105].

Coprinellus, belonging to the phylum Basidiomycota and family Psathyrellaceae, was also explored for its various bioactive compounds, including its nutritional profile, polysaccharides, phenolic compounds, macroelements, microelements, fatty acids, and proteins, among others. According to Badalyan^[30], many coprinoid mushrooms produce bioactive compounds, including polysaccharides, phenolics, and terpenoids, which have various beneficial effects, such as antimicrobial activity, immune modulation, antioxidant properties, cell growth stimulation, nematocidal activity, and antidiabetic activity. In the present review, 51 bioactive compounds, including sugar alcohol (one), fatty acids (four), phenolic compounds (six), flavonoids (22), hydroxycinnamic acid and derivatives (six), coumarins (three), organic acids (two), sugars (two), and sesquiterpenes (five) were recorded in eight species of Coprinellus, specifically C. curtus, C. disseminatus, C. domesticus, C. ellisii, C. micaceus, C. radians, C. truncorum, and C. xanthorix (Table 2). Additionally, in the study of Novaković et al.^[44], the determination of amino acid composition, fatty acid profile, and mineral composition of C. dessiminatus was also recorded. Based on their findings, 17 amino acids (essential and non-essential), seven fatty acids (polyunsaturated, saturated, monounsaturated), three macroelements (K, Mg, and Ca), and four microelements (Cu, Zn, Mn, and Fe) were present in the methanolic extract of C. disseminatus. The total essential amino acids were 29.57 mg/g DW, with leucine being the most abundant, while non-essential amino acids totaled 96.69 mg/g DW. In addition, fatty acids consisted of 59.1% polyunsaturated, 23.1% saturated, and 17.9% monounsaturated, primarily linoleic (56.6%), palmitic (13.9%), and oleic acids (12.0%). Potassium was the most abundant macroelement, followed by calcium and magnesium, while iron dominated microelements^[44].

Furthermore, an in vitro study by Novaković et al.^[106] on the antiproliferative effects of C. disseminatus against the MCF-7 breast cancer cell line indicated a strong correlation between the total phenolic and flavonoid content and the cytotoxic activity. Therefore, C. disseminatus could be considered a potential alternative source of nutraceuticals and biologically active compounds. Likewise, Coprinsesquiterpenes, a new bisabolene-type sesquiterpene extracted from Coprinellus mushrooms, demonstrated anti-inflammatory effects, with IC₅₀ values ranging from 12.8 μM to 34.7 μM in the Nitric Oxide (NO) inhibition assay^[107]. Likewise, both the polysaccharides (PSH) and exopolysaccharides (ePSH) of C. truncorum demonstrated notable cytotoxic effects on human-derived HepG2 cancer cells^[108].

Furthermore, aside from characterization, these bioactive compounds were also evaluated for diverse biological activities. According to Eguchi et al.^[109], mushrooms contain various bioactive compounds with diverse health benefits, including antiviral, antidiabetic, antiparasitic, antibacterial, anti-hypercholesterolemic, and anticancer properties. Additionally, these compounds exhibit hepatoprotective, cardiovascular, energy-boosting, immune-modulating, and antioxidant effects. These advantageous properties are primarily attributed to the cellular components and secondary metabolites present in mushrooms, particularly those belonging to Basidiomycota^[110]. Moreover, as noted by Ghora et al.^[111], these medicinal properties are primarily derived from the fruiting body, culture mycelium, and culture broth of mushroom species.

Accordingly, the bioactivities of Coprinellus mushrooms, including C. disseminatus, C. micaceus, and C. truncorum, were assessed using different extracts and isolated bioactive compounds (Table 3). Notably, Coprinellus mushrooms exhibited 12 different bioactivities, including antifungal, promoting seed germination, biobleaching, antiproliferative, antioxidant, cytotoxic, lignocellulolytic, biotransformation of polychlorinated dibenzo-p-dioxin, antidiabetic, anticholinesterase, anti-tyrosinase, and anti-inflammatory properties. For instance, the study by Nguyen et al.^[91] evaluated four different bioactivities, specifically antidiabetic, antioxidant, tyrosinase, and NO inhibitory activities, as well as anticholinesterase activity, of the methanol and hot water extracts of the fruiting body of C. micacues. Accordingly, studies have revealed that the fruiting body of C. micaceus contains bioactive compounds exhibiting anti-inflammatory, antioxidant, α-glucosidase inhibitory, anti-tyrosinase, and anti-acetylcholinesterase activities, indicating their potential use in the pharmaceutical industry^[91].

In summary, mushrooms, including species from the genus Coprinellus, are valuable sources of bioactive compounds with significant nutritional and medicinal potential. However, despite their promising applications in the pharmaceuticals, nutraceuticals, and food industries, research on Coprinellus remains limited, with only a few species being studied for their biochemical composition and bioactivities. The existing studies reveal that Coprinellus species contains essential amino acids, fatty acids, polysaccharides, phenolic compounds, and minerals, while also exhibiting diverse bioactivities, including antioxidant, antimicrobial, antidiabetic, and anti-inflammatory effects. Nevertheless, the full scope of their medicinal and nutritional benefits remains underexplored due to the lack of comprehensive research on most species within this genus. Thus, to fully utilize the potential of Coprinellus mushrooms, further biochemical and bioactivity studies are recommended on a broader range of species within this genus. Expanding research efforts will not only enhance the understanding of the medicinal and nutritional properties but also uncover novel bioactive compounds that could be utilized in various industries.

This review highlighted the distribution, biological compounds, and bioactivity of Coprinellus species worldwide. It presents a comprehensive checklist of 67 Coprinellus species, 51 different bioactive compounds, and 12 different bioactivities. The documented compounds and bioactivities establish an important foundation for the effective use of Coprinellus mushrooms in the nutraceutical and pharmaceutical industries. However, despite their rich bioactive potential, only eight species have been studied in detail.

Therefore, based on the compiled data, the following areas should be prioritized in future research:

(1) Conduct thorough studies on Coprinellus species, ensuring accurate characterization and classification using both morphological and molecular approaches.

(2) Additional species listing and optimization studies, especially for those countries with an ideal growing environment, favoring the growth of Coprinellus utilizing agro-industrial wastes and other cost-effective, locally available substrates.

(3) Isolate, characterize, and identify novel biological compounds in understudied and newly discovered Coprinellus species.

(4) Investigate additional biological activities across different models and elucidate their mechanism of action,

(5) Assess the edibility of various species of Coprinellus mushrooms through comprehensive chemical and toxicological analysis.

(6) Develop Coprinellus-based products, including functional foods, dietary supplements, and pharmaceutical drugs.