Schizophyllum commune
1. Classification
a. Higher order taxa
Eukaryota (Domain); Opisthokonta (Clade); Fungi (Kingdom); Dikarya (Sub-kingdom); Basidiomycota (Phylum); Agaricomycotina (Subphylum); Agaricomycetes (Class); Agaricomycetidae (Subclass); Agaricales (Order); Schizophyllineae (Suborder); Schizophyllaceae (Family); Schizophyllum (Genus)
Species: Schizophyllum commune
Common name: Split Gill Mushroom
2. Description and Significance
Schizophyllum commune, commonly referred to as the split gill mushroom, is a fungus with white, fan-shaped caps and distinctive split gills underneath. S. commune is found in all continents except Antarctica, and plays a crucial role in ecosystems by recycling nutrients into the soil via decomposition. S. commune has a complex pathogenic nature: because it is capable of digesting lignocellulose, a polysaccharide compound present in the cell walls of woody plants, it is considered a plant parasite, leading to root-rot in various types of trees. It is capable of degrading a variety of polysaccharides [1]; however, there is currently controversy as to whether S. commune should be classified as a brown-rot or white-rot fungus.
S. commune is considered a model fungus for study, given its relatively quick 10-day life cycle and that it has had its entire genome sequenced [1]. These factors have attracted many researchers to it for medical applications as an antioxidant, immune system booster, and environmental applications as a chemical insecticide. On the other hand, S. commune is also considered a potential human pathogen implicated in various pulmonary conditions, however its effect on human health and possible treatments is still debated.
3. Genome structure
Schizophyllum commune’s genome, sequenced from the H4-8 strain, is 38.5 megabases and consists of 14 chromosomes, containing 13,210 genes from which 11.2% are repeated sequences. There is a large proportion of coding sequences (4,859 genes) with an average length of 1794.91 base pairs and about 5.7 exons per gene. The average protein length is 447.8 amino acids [1]. 39% of S. commune’s proteins have orthologs (genes found in different species that evolved from a common ancestor) across the Dikarya fungi subkingdom, while 36% of the proteins are characteristic of S. commune; however, a considerable amount of its proteome remains uncharacterized [1].
A recent discovery is S. commune’s capacity to degrade plant cell wall compounds including lignocellulose. The machinery it uses for this process is composed of lignin-degrading enzymes known as FOLymes, which encompasses lignin-degrading auxiliary enzymes (LDA family) and lignin oxidases (LO family) [1]. S. commune possesses 16 FOLyme genes and 11 complementary genes that are distant relatives of the FOLymes (lignin-degrading auxiliary enzymes and oxidases). However, S. commune lacks lignin peroxidases (LO2 family) that are important enzymes for the degradation of lignin, a rigid material necessary for plant support and strength, limiting its capacity for lignin elimination [1], [2]. Little is still known about the extracellular enzyme system that S. commune secretes during the breakdown of lignocellulose, and its underlying degradation mechanism is not well understood [2]. Therefore, there is controversy as to whether S. commune fits under the brown-rot or white-rot fungi classification; nevertheless, a study suggests it is an intermediate between both [2]. Regardless, the S. commune genome encodes one of the highest numbers of cellulose, hemicellulose, pectin, and other polysaccharide degrading enzymes compared to other genomes of its phylum [1].
4. Cell structure
The chemical structure of the S. commune’’ wall has been identified using ssNMR spectroscopy, liquid chromatography, and glycosyl linkage analysis. The cell wall consists of different polysaccharide types of α- and β-(1,3)-glucans, β-(1,4)-chitin, and mannose [3]. The rigid part of the cell wall comprises various chitin forms and glucans, while the more flexible part contains terminal hexoses and different mannoses [3].
The identification of fucose in the inner core of the cell wall, even after alkali treatment, is unusual for major fungal phyla. The presence of α-(1,3)-glucan in the core suggests it is a potential target for antifungal treatments, and the newly discovered fucose may also be a candidate for antifungal development. Contrary to previous studies, analyses found no evidence of peptides involved in polysaccharide cross-connections in the S. commune cell wall [3]. In the future, more advanced NMR techniques may refine our understanding of the cell wall's molecular structure.
5. Metabolism
S. commune can decompose the biomass of more than 150 different plant species, where cellulose, hemicellulose and pectin serve as its primary carbon source [1]. This chemoheterotrophic fungus typically infiltrates wood through the xylem rays, which are special channels that allow water and nutrients to spread through the plant. To initiate the breakdown of these molecules, the fungus invades the plant’s vessels and parenchymatic cells; these cells are part of the plant’s ground tissue and serve for nutrient storage. To accomplish this process, S. commune produces 366 carbohydrate-active enzymes known as CAZymes, where 106 of them are involved in polysaccharide degradation [2]. S. commune possesses the highest β-glucosidase activity (cellulose degrading-enzymatic activity) in comparison to other white-rot and brown-rot fungi [2].
S. commune often requires oxygen for its development; however, it can also be found in deep subseafloor sedimentary environments, having the ability to produce energy in the absence of oxygen [4], [5]. The fungus does this by fermenting glucose, producing ethanol, and later on, using it as an alternative carbon source [4]. Consequently, S. commune can conduct both aerobic and anaerobic respiration, and this serves as a possible explanation for the species’ global distribution [5]. Nevertheless, when S. commune encounters anaerobic environments, it produces morphological changes such as undergrown fruit-bodies as a mechanism to cope with the hypoxic conditions. This is due to the downregulation of expression of genes necessary for the production of a mature fruit body [5].
6. Ecology
S. commune is found globally growing on the bark of trees, which it uses as a substrate for metabolism. Although it is found in many different environments, it has an optimal growth temperature around 30-35 °C, and an optimal growth pH of 5 [6].
S. commune contains an extensive toolkit for degrading lignocellulose, a large component of plant cell walls, especially in trees [1]. S. commune is known to degrade the bark of fruiting trees, however it has also been seen to rot the fruit itself [7], suggesting it is capable of obtaining nutrients from more plant sources.
When co-inoculated with different bacteria, S. commune shows varied responses; commonly reduced growth of the fungus via an antagonistic reaction from the bacteria, with some even being able to grow along the hyphae when it comes in contact with the colony [8].
When grown with different fungi, three main responses are seen: deadlock when grown with F. velutipes, replacement when grown with S. lacrymans, and induction of S. commune fruiting bodies when grown with G. lucidum [8]. Deadlock is a relationship seen in competing fungi where neither is able to outgrow the other. Replacement is where one fungus completely takes over the other, resulting in complete control over the limited resources. Finally, induction of fruiting bodies is an interaction that promotes growth of one fungus, as fruiting bodies contain spores used for reproduction [8]. This interaction is similar to what is seen with normal S. commune growth on wood.
7. Pathology
Although S. commune is used as a food source in Asia and Africa, recent research shows that S. commune may be involved in fungal rhinosinusitis and other respiratory or pulmonary conditions [1], [9], [10].
Since the first well-documented pulmonary infection caused by S. commune in 1994, there has been an increasing number of reports of infections caused by S. commune in both people with strong immune systems (immunocompetent) and those with weakened immune systems (immunocompromised) [10]. The optimal approach for S. commune infections remains uncertain due to their rarity, with no consensus on treatment options. Chronic non-invasive sinusitis can affect immunocompetent individuals without invading mucosal or blood vessels. At the same time, the invasive forms of the infection typically occur in immunocompromised individuals and involve tissue and vascular invasion [10].
In a 1994 case, a 58-year-old patient was admitted to a medical center due to progressive muscle weakness. Lung tissue cultures confirmed the presence of S. commune. Despite treatment, the patient's condition deteriorated resulting in his death. While the most efficacious treatment remains uncertain, surgical drainage, debridement, and antifungal therapy have succeeded [9].
S. commune is also a known pathogen of wood, as it is considered a wood-rot pathogen of fruit trees, ornamental trees, and lumber trees [11]. Some targets of S. commune’s pathogenicity are Ulmus sp. (elm), Tilia sp. (lime), Fagus sp. (beech), Picea rubens (red spruce), Prunus salicina (Japanese plum), and ornamental Prunus sp. [11]. Once infected by S. commune, the woody substrate colonized often becomes discolored. S. commune can more easily colonize a tree if the tree has a wound such as from pruning, a freeze injury, a sunscald lesion, a lesion from a different pathogen, a fire, or if there is already a dead branch stub on the tree [11]. It may be possible to control S. commune infection by spraying trees against other microbes, since S. commune can more easily colonize wood if there is already damage present from other pathogens [11].
8. Applications
Due to its polysaccharide degrading capacity, S. commune has a variety of applications including the production of enzymatic cocktails, usage for pollutant degradation, and biofuel manufacture [1], [2], [12]. Additionally, S. commune is used for the synthesis of schizophyllan, a water soluble polysaccharide composed of anhydroglucose molecules with glucose side chains [13]. This compound is often utilized in cosmetic and pharmaceutical products as a bioactive ingredient [13].
Safer and more environmentally friendly options to chemical insecticides are in high demand and is a developing field. A specific application of S. commune is its insecticidal effects against Spodptera litura and its potential to be a more eco-friendly alternative to chemical insecticides [14]. When larvae were treated with S. commune fungal extract as opposed to other fungal extracts, they experienced the highest number of apoptotic and necrotic cells and had little recovery [14]. These results confirm that S. commune is both non toxic and provides long term treatment effects [14].
Lastly, using statistical analysis and optimization of conditions for enzymatic processes, it was found that S. commune may have medicinal characteristics [15]. S. commune possesses vital antioxidant properties that diminish the effects of harmful free radicals in the body, and these properties have the potential to reduce the risk of diseases such as cancer and heart disease [15]. S. commune was investigated for the presence of vitamins like B, C, D, and K and minerals such as potassium and phosphorus, and all nutrients were found in abundance. When S. commune is broken down, it releases these nutrients that in turn benefit the body in preventing and reducing the risk of fatal diseases [15].
9. Current Research
Much of the current research on S. commune focuses on its potential effects on the immune system. Researchers have investigated the immune effects of polysaccharides isolated from S. commune [16]. They focused their efforts on macrophages, which are molecules in the body that can engulf pathogens and release chemical messengers called cytokines to mediate an immune response. In the study, mouse macrophage cells were cultured with the polysaccharide isolated from S. commune [16]. It was found that the polysaccharide significantly increased the macrophages’ production of chemicals that can kill pathogens. Additionally, the polysaccharide caused an increase of anti-inflammatory cell signals to be produced by the macrophage cells. This finding shows that polysaccharides isolated from S. commune have the potential to enhance macrophage cells’ natural immunity [16].
Similar experiments were performed in order to elucidate the role of β-glucans isolated from S. commune on mouse macrophage cell activity [17]. β-glucans are polysaccharides found in the cell walls of bacteria and fungi. The murine macrophage cells were exposed to a lipopolysaccharide from A. actinomycetemcomitans, which is a pathogen known to cause periodontitis, or gum disease [17]. Periodontitis is characterized by excess inflammation in the gums due to the presence of various pathogens. When β-glucans bind to their target receptor on macrophage cells, they cause the macrophage cells to release both inflammatory and anti-inflammatory messages, along with reactive oxygen species which can kill the pathogen. The researchers pre-treated mouse macrophage cells with β-glucans from S. commune and subsequently cultured the cells with a lipopolysaccharide isolated from A. actinomycetemcomitans. In response, the macrophage cells significantly increased their production of anti-inflammatory chemical messengers, and it was found that Dectin-1 was the main receptor being activated in this process [17]. This finding shows that β-glucans from S. commune have the potential to help incite an anti-inflammatory response in periodontal disease.
10. References
[1] [Ohm, R., de Jong, J., Lugones, L. et al. (2010). Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28, 957–963. https://doi.org/10.1038/nbt.1643.]
[2] [Zhu, N., Liu, J., Yang, J., Lin, Y., Yang, Y., Ji, L., Li, M., & Yuan, H. (2016). Comparative analysis of the secretomes of Schizophyllum commune and other wood-decay basidiomycetes during solid-state fermentation reveals its unique lignocellulose-degrading enzyme system. Biotechnol Biofuels 9. https://doi.org/10.1186/s13068-016-0461-x]
[3] [Ehren, H. L., Appels, F. V. W., Houben, K., Renault, M. A. M., Wösten, H. A. B., & Baldus, M. (2020). Characterization of the cell wall of a mushroom forming fungus at atomic resolution using solid-state NMR spectroscopy. The Cell Surface, 6, 100046. https://doi.org/10.1016/j.tcsw.2020.100046]
[4] [Arifeen, M. Z. U., Chu, C., Yang, X., Liu, J., Huang, X., Ma, Y., Liu, X., Xue, Y., & Liu, C. (2020). The anaerobic survival mechanism of Schizophyllum commune 20R-7-F01, isolated from deep sediment 2 km below the seafloor. Environmental Microbiology: Special Issue on Advances in Environmental Microbiology in China, 23(2). https://doi.org/10.1111/1462-2920.15332]
[5] [Liu, C-H., Huang, X., Xie, T-N., Duan, N., Xue, Y-R., Zhao, T-X., Lever, M. A., Hinrichs, K-U., & Inagaki, F. (2016). Exploration of cultivable fungal communities in deep coal-bearing sediments from ∼1.3 to 2.5 km below the ocean floor. Environmental Microbiology, 16(2). https://doi.org/10.1111/1462-2920.13653]
[6] [Imtiaj A, Jayasinghe C, Lee GW, et al. Physicochemical requirement for the vegetative growth of Schizophyllum commune collected from different ecological origins. Mycobiology. 2008;36(1):34. doi:10.4489/myco.2008.36.1.034]
[7] [Latham AJ. Development of apple fruit rot and basidiocarp formation by Schizophyllum commune. Phytopathology. 1970;60(4):596. doi:10.1094/phyto-60-596]
[8] [Krause K, Jung EM, Lindner J, et al. Response of the wood-decay fungus Schizophyllum commune to co-occurring microorganisms. ‘’PLoS One’’ 2020;15(4):e0232145. Published 2020 Apr 23. doi:10.1371/journal.pone.0232145]
[9] [Rihs, J. D., Padhye, A. A., & Good, C. B. (1996). Brain abscess caused by Schizophyllum commune: an emerging basidiomycete pathogen. Journal of Clinical Microbiology, 34(7), 1628–1632. https://doi.org/10.1128/jcm.34.7.1628-1632.1996]
[10] [Swain, B., Panigraphy, R,. & Panigrahi, D. (2011). Schizophyllum commune sinusitis in an immunocompetent host. Indian Journal of Medical Microbiology, 29(4), 439-442]
[11] [Takemoto, Nakamura, H., Erwin, Imamura, Y., & Shimane, T. (2010). Schizophyllum commune as a Ubiquitous Plant Parasite. JARQ. Japan Agricultural Research Quarterly, 44(4), 357–364. https://doi.org/10.6090/jarq.44.357]
[12] [Tovar-Herrera, O. E., Martha-Paz, A. M., Pérez-LLano, Y., Aranda, E., Tacoronte-Morales, J. E., Pedroso-Cabrera, M. T., Arévalo-Niño, K., Folch-Mallol, J. L., & Batista-García, R. A. (2018). Schizophyllum commune: An unexploited source for lignocellulose degrading enzymes. MicrobiologyOpen, 7(3), e00637. https://doi.org/10.1002/mbo3.637]
[13] [Kumar, A., Bharti, A. K., and Bezie, Y. (2022). Schizophyllum commune: A fungal cell-factory for production of valuable metabolites and enzymes. BioResources 17(3), 5420-5436. https://bioresources.cnr.ncsu.edu/resources/schizophyllum-commune-a-fungal-cell-factory-for-production-of-valuable-metabolites-and-enzymes/]
[14] [Kaur, M., Chadha, P., Kaur, S. et al. Schizophyllum commune induced genotoxic and cytotoxic effects in Spodoptera litura. Sci Rep 8, 4693 (2018). https://doi.org/10.1038/s41598-018-22919-0]
[15] [Wongaem, A., Reamtong, O., Srimongkol, P., Sangtanoo, P., Saisavoey, T., & Karnchanatat, A. (2021). Antioxidant properties of peptides obtained from the split gill mushroom (Schizophyllum commune). Journal of food science and technology, 58(2), 680–691.]
[16] [Yelithao, Surayot, U., Lee, C., Palanisamy, S., Prabhu, N. M., Lee, J., & You, S. (2019). Studies on structural properties and immune-enhancing activities of glycomannans from Schizophyllum commune. Carbohydrate Polymers, 218, 37–45. https://doi.org/10.1016/j.carbpol.2019.04.057]
[17] [Thongsiri, Nagai-Yoshioka, Y., Yamasaki, R., Adachi, Y., Usui, M., Nakashima, K., Nishihara, T., & Ariyoshi, W. (2021). Schizophyllum commune β-glucan: Effect on interleukin-10 expression induced by lipopolysaccharide from periodontopathic bacteria. Carbohydrate Polymers, 253, 117285–117285. https://doi.org/10.1016/j.carbpol.2020.117285]
Edited by [Alexandria Barnes, Ana C. Carrera Barrera, Jamie Chamberlain, Luciano Foranoce, Julia Fulfaro], students of [mailto:jmbhat@bu.edu Jennifer
Bhatnagar] for [http://www.bu.edu/academics/cas/courses/cas-bi-311/ BI 311
General Microbiology], 2023, Boston University.
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Bhatnagar at Boston University]]
