Taxonomy of rock-inhabiting fungi from James Ross Island, Antarctica
Vol.13,No.1(2023)
A total of 51 strains of rock-inhabiting fungi, which were isolated from rock fragments in the deglaciated area of James Ross Island, Antarctica, were studied and compared by sequencing the ITS rDNA region. Analysed strains were classified into two classes of the phylum Ascomycota. Specifically, 41 strains were classified within the families Teratosphaeriaceae (20) and Extremaceae (21), belonging to the order Mycosphaerellales of the class Dothideomycetes. The remaining Dothideomycetes strains were found to be related to species from the orders Cladosporiales and Dothideales. Additionally, only four strains were related to the order Chaetothyriales, which belongs to the class Eurotiomycetes. On the whole, 29 analysed strains were affiliated with four genera of typical rock-inhabiting fungi, namely Oleoguttula, Rachicladosporium, Elasticomyces and Vermiconidia. The genus Vermiconidia was represented by the highest number of isolates among the studied strains, suggesting that it represents a common component of the fungal community of the investigated area. Out of the 51 analysed strains, only seven were successfully identified as the species Rachicladosporium antarcticum, Oleoguttula mirabilis, and Elasticomyces elasticus. Further investigation and characterization of the majority of analysed strains are necessary to determine their taxonomic position and describe potentially new taxa.
Antarctica; black yeast; ITS rDNA region; Dothideomycetes; meristematic fungi; microcolonial fungi; rock-inhabiting fungi
Abdollahzadeh, J., Groenewald, J. Z., Coetzee, M. P. A., Wingfield, M. J. and Crous, P. W. (2020): Evolution of lifestyles in Capnodiales. Studies in Mycology, 95: 381-414. doi: 10.1016/j.simyco.2020.02.004
Ametrano, C. G., Knudsen, K., Kocourková, J., Grube, M., Selbmann, L. and Muggia, L. (2019): Phylogenetic relationships of rock-inhabiting black fungi belonging to the widespread genera Lichenothelia and Saxomyces. Mycologia, 111(1): 127-160. doi: 10.1080/00275514.2018.1543510
Coleine, C., Selbmann, L. (2021): 2.1 Black fungi inhabiting rock surfaces. In: B. Büdel, T. Friedl (eds.): Life at Rock Surfaces: Challenged by Extreme Light, Temperature and Hydration Fluctuations. Berlin, Boston: De Gruyter, pp. 57–86. doi: 10.1515/9783110646467-003
Coleine, C., Stajich, J. E., De Los Ríos, A. and Selbmann, L. (2021): Beyond the extremes: Rocks as ultimate refuge for fungi in drylands. Mycologia, 113(1): 108-133. doi: 10.1080/00275514.2020.1816761
Coleine, C., Zucconi, L., Onofri, S., Pombubpa, N., Stajich, J. and Selbmann, L. (2018): Sun exposure shapes functional grouping of fungi in cryptoendolithic Antarctic communities. Life, 8(2): 19. doi: 10.3390/life8020019
Connell, L., Staudigel H. (2013): Fungal diversity in a Dark Oligotrophic Volcanic Ecosystem (DOVE) on Mount Erebus, Antarctica. Biology, 2(2): 798-809. doi: 10.3390/biology2020798.
Costa, F. F., Da Silva, N. M., Voidaleski, M. F., Weiss, V. A., Moreno, L. F., Schneider, G. X., Najafzadeh, M. J., Sun, J., Gomes, R. R., Raittz, R. T., Castro, M. A. A., De Muniz, G. B. I., De Hoog, G. S. and Vicente, V. A. (2020): Environmental prospecting of black yeast-like agents of human disease using culture-independent methodology. Scientific Reports, 10(1): 14229. doi: 10.1038/s41598-020-70915-0
Crous, P. W., Groenewald, J. Z. (2011): Why eternities don't last. Persoonia, 26: 70-84.
Crous, P. W., Schumacher, R. K., Akulov, A., Thangavel, R., Hernández-Restrepo, M., Carnegie, A. J., Cheewangkoon, R., Wingfield, M. J., Summerell, B. A., Quaedvlieg, W., Coutinho, T. A., Roux, J., Wood, A. R., Giraldo, A. and Groenewald, J. Z. (2019a): New and interesting fungi. 2. Fungal Systematics and Evolution, 3: 57-134.
Crous, P. W., Summerell, B. A., Mostert, L. and Groenewald, J. Z. (2008): Host specificity and speciation of Mycosphaerella and Teratosphaeria species associated with leaf spots of Proteaceae. Persoonia, 20: 59-86.
Crous, P. W., Wingfield, M. J., Lombard, L., Roets, F., Swart, W. J., Alvarado, P., Carnegie, A. J., Moreno, G., Luangsaard, J., Thangavel, R., Alexandrova, A. V., Baseia, I. G., Bellanger, J. M., Bessette, A. E., Bessette, A. R., De La Peña-Lastra, S., García, D., Gené, J., Pham, T. H. G., Heykoop, M. et al. (2019b): Fungal Planet description sheets: 951–1041. Persoonia, 43: 223-425. doi: 10.3767/persoonia.2019.43.06
De Hoog, G. S., Guarro, J., Gené, D. J., Ahmed, S. A., Al-Hatmi, A. M. S., Figueras, M. J. and Vitale, R. G. (2020): Atlas of clinical fungi. 4th edition. Hilversum: Foundation Atlas of Clinical Fungi, 779 p.
De Hoog, G. S., Hermanides-Nijhof, E. (1977): The black yeasts and allied Hyphomycetes. Studies in Mycology, 15: 1-222.
Egidi, E., De Hoog, G. S., Isola, D., Onofri, S., Quaedvlieg, W., De Vries, M., Verkley, G. J. M., Stielow, J. B., Zucconi, L. and Selbmann, L. (2014): Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multilocus phylogenies. Fungal Diversity, 65: 127-165.
Felsenstein, J. (1985): Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39: 783-791.
Gostinčar, C., Ohm, R. A., Kogej, T., Sonjak, S., Turk, M., Zajc, J., Zalar, P., Grube, M., Sun, H., Han, J., Sharma, A., Chiniquy, J., Ngan, C. Y., Lipzen, A., Barry, K., Grigoriev, I. V. and Gunde-Cimerman, N. (2014): Genome sequencing of four Aureobasidium pullulans varieties: Biotechnological potential, stress tolerance, and description of new species. BMC genomics, 15: 549. doi: 10.1186/1471-2164-15-549
Gueidan, C., Villaseñor, C. R., De Hoog, G. S., Gorbushina, A. A., Untereiner, W. A. and Lutzoni, F. (2008): A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Studies in Mycology, 61: 111-119. doi: 10.3114/sim.2008.61.11
Hubka, V., Réblová, M., Rehulka, J., Selbmann, L., Isola, D., De Hoog, S. G. and Kolařík, M. (2014): Bradymyces gen. nov. (Chaetothyriales, Trichomeriaceae), a new ascomycete genus accommodating poorly differentiated melanized fungi. Antonie van Leeuwenhoek, 106(5): 979-992. doi: 10.1007/s10482-014-0267-4
Huelsenbeck, J. P., Ronquist, F. (2001): MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17: 754-755.
Isola, D., Zucconi, L., Onofri, S., Caneva, G., De Hoog, G. S. and Selbmann, L. (2015): Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Diversity, 76: 75-96.
Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K. (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35: 1547-1549.
Laichmanová, M. (2020): New records of Oleoguttula mirabilis and Rachicladosporium antarcticum from James Ross Island, Antarctica. Czech Polar Reports, 10(2): 226-235. doi: 10.5817/CPR2020-2-17
Martin-Sanchez, P. M., Gebhardt, C., Toepel, J., Barry, J., Munzke, N., Günster, J. and Gorbushina, A. A. (2018): Monitoring microbial soiling in photovoltaic systems: A qPCR-based approach. International Biodeterioration and Biodegradation, 129: 13-22.
Marvanová, L., Laichmanová, M. (2014): Campylospora leptosoma sp. nov. and characteristics of Campylospora spp., based on morphology and on ITS sequences. Mycosphere, 5(2): 245-261.
Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T. L., Agarwala, R. and Schäffer, A. A. (2008): Database indexing for production MegaBLAST searches. Bioinformatics, 24(16): 1757-1764. doi: 10.1093/bioinformatics/btn322
Muggia, L., Fleischhacker, A., Kopun, T. and Grube, M. (2016): Extremotolerant fungi from alpine rock lichens and their phylogenetic relationships. Fungal Diversity, 76: 119-142. doi: 10.1007/s13225-015-0343-8
Muggia, L., Quan, Y., Gueidan, C., Al-Hatmi, A. M. S., Grube, M. and De Hoog, S. (2021): Sequence data from isolated lichen-associated melanized fungi enhance delimitation of two new lineages within Chaetothyriomycetidae. Mycological Progress, 20: 911-927. doi: 10.1007/ s11557-021-01706-8
Nei, M., Kumar, S. (2000): Molecular Evolution and Phylogenetics. Oxford University Press. Oxford, 333 p.
Nepel, M., Voglmayr, H., Schönenberger, J. and Mayer, V. E. (2014): High diversity and low specificity of chaetothyrialean fungi in carton galleries in a neotropical ant-plant association. PloS One, 9(11): e112756. doi: 10.1371/journal.pone.0112756
Nylander, J. A. A. (2004): MrModeltest v2. Program distributed by the author.
Perini, L., Gostinčar, C., Anesio, A. M., Williamson, C., Tranter, M. and Gunde-Cimerman, N. (2019): Darkening of the Greenland Ice Sheet: Fungal abundance and diversity are associated with algal bloom. Front Microbiology, 10: 557. doi: 10.3389/fmicb.2019.00557
Prasongsuk, S., Lotrakul, P., Ali, I., Bankeeree, W. and Punnapayak, H. (2018): The current status of Aureobasidium pullulans in biotechnology. Folia Microbiologica, 63(2): 129-140. doi: 10.1007/s12223-017-0561-4
Quaedvlieg, W., Binder, M., Groenewald, J. Z., Summerell, B. A., Carnegie, A. J., Burgess, T. I. and Crous, P. W. (2014): Introducing the Consolidated Species Concept to resolve species in the Teratosphaeriaceae. Persoonia Molecular Phylogeny and Evolution of Fungi, 33: 1-40.
Quan, Y., Muggia, L., Moreno, L. F., Wang, M., Al-Hatmi, A. M. S., da Silva Menezes, N., Shi, D., Deng, S., Ahmed, S., Hyde, K. D., Vicente, V. A., Kang, Y., Stielow, J. B. and de Hoog, S. (2020): A re-evaluation of the Chaetothyriales using criteria of comparative biology. Fungal Diversity, 103: 47-85. doi: 10.1007/s13225-020-00452-8
Ruibal, C., Gueidan, C., Selbmann, L., Gorbushina, A. A., Crous, P. W., Groenewald, J. Z., Muggia, L., Grube, M., Isola, D., Schoch, C. L., Staley, J. T., Lutzoni, F. and De Hoog, G. S. (2009): Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Studies in Mycology, 64: 123-133.
Ruibal, C., Platas, G. and Bills, G. F. (2005): Isolation and characterization of melanized fungi from limestone formation in Mallorca. Mycological Progress, 4: 23-38.
Ruibal, C., Platas, G. and Bills, G. F. (2008). High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia, 21: 93-110. doi: 10.3767/003158508X371379
Ruibal, C., Selbmann, L., Avci, S., Martin-Sanchez, P. and Gorbushina, A. (2018): Roof-inhabiting cousins of rock-inhabiting fungi: Novel melanized microcolonial fungal species from photocatalytically reactive subaerial surfaces. Life, 8(3): 30. doi: 10.3390/life8030030
Sánchez, R. M., Miller, A. N. and Bianchinotti, M. V. (2019): New species of Capronia (Herpotrichiellaceae, Ascomycota) from Patagonian forests, Argentina. Plant and Fungal Systematics, 64(1): 81-90.
Selbmann, L., De Hoog, G. S., Mazzaglia, A., Friedmann, E. I. and Onofri, S. (2005): Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Studies in Mycology, 51: 1-32.
Selbmann, L., De Hoog, G. S., Zucconi, L., Isola, D., Ruisi, S., Gerrits Van Den Ende, A. H., Ruibal, C., De Leo, F., Urzì, C. and Onofri, S. (2008): Drought meets acid: Three new genera in a dothidealean clade of extremotolerant fungi. Studies in Mycology, 61: 1-20.
Selbmann, L., Grube, M., Onofri, S., Isola, D. and Zucconi, L. (2013): Antarctic epilithic lichens as niches for black meristematic fungi. Biology, 2(2): 784-797. doi: 10.3390/ biology2020784
Selbmann, L., Onofri, S., Zucconi, L., Isola, D., Rottigni, M., Ghiglione, C., Piazza, P., Alvaro, M. C. and Schiaparelli, S. (2015): Distributional records of Antarctic fungi based on strains preserved in the Culture Collection of Fungi from Extreme Environments (CCFEE) Mycological Section associated with the Italian National Antarctic Museum (MNA). MycoKeys, 10: 57-71. doi: 10.3897/mycokeys.10.5343
Sert, H. B., Sümbül, H. and Sterflinger, K. (2007): Microcolonial fungi from antique marbles in Perge/Side/Termessos (Antalya/Turkey). Antonie Van Leeuwenhoek, 91: 217-227.
Sert, H. B., Wuczkowski, M. and Sterflinger, K. (2012): Capnobotryella isiloglui, a new rock-inhabiting fungus from Austria, Turkish Journal of Botany, 36(4): 401-407. doi: 10.3906/bot-1102-3
Staley, J. T., Palmer, F. and Adams, J. B. (1982): Microcolonial fungi: Common inhabitants on desert rocks? Science, 215 (4536): 1093-1095. doi: 10.1126/science.215.4536.1093.
Sterflinger, K. (1998): Temperature and NaCl- tolerance of rock-inhabiting meristematic fungi. Antonie Van Leeuwenhoek, 74: 271-281.
Sterflinger, K. (2006): Black yeasts and meristematic fungi: ecology, diversity and identification. In: G. Péter, C. A. Rosa (eds.). Biodiversity and Ecophysiology of Yeasts. The Yeast Handbook. Springer, Berlin, Heidelberg, pp. 501–514.
Sterflinger, K., De Hoog, G. S. and Haase, G. (1999): Phylogeny and ecology of meristematic ascomycetes. Studies in Mycology, 43: 5-22.
Sterflinger, K., Krumbein, W. E. (1995): Multiple stress factors affecting growth of rock-inhabiting black fungi. Botanica Acta, 108(6): 490-496. doi: 10.1111/j.1438-8677.1995. tb00526.x
Sterflinger, K., Tesei, D. and Zakharova, K. (2012): Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecology, 5(4): 453-462. doi: 10.1016/ j.funeco.2011.12.007
Sun, W., Su, L., Yang, S., Sun, J., Liu, B., Fu, R., Wu, B., Liu, X., Cai, L., Guo, L. and Xiang, M. (2020): Unveiling the hidden diversity of rock-inhabiting fungi: Chaetothyriales from China. Journal of Fungi, 6(4): 187. doi: 10.3390/jof6040187
Swofford, D. L. (2003): PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland.
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994): CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673-4680.
Tsurykau, A., Etayo, J. (2017): Capronia suijae (Herpotrichiellaceae, Eurotiomycetes), a new fungus on Xanthoria parietina from Belarus, with a key to the lichenicolous species growing on Xanthoria s. str. The Lichenologist, 49(1): 1-12. doi: 10.1017/S0024282916000530
Vasse, M., Voglmayr, H., Mayer, V., Gueidan, C., Nepel, M., Moreno, L., De Hoog, S., Selosse, M-A, Mckey, D. and Blatrix, R. (2017): A phylogenetic perspective on the association between ants (Hymenoptera: Formicidae) and black yeasts (Ascomycota: Chaetothyriales). Proceedings of the Royal Society B, 284: 20162519. doi: 10.1098/rspb.2016. 2519
Vilgalys, R., Hester, M. (1990): Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriolog, 172: 4238-4246.
White, T. J., Bruns, T., Lee, S. and Taylor, J. W. (1990): Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White (eds.): PCR protocols: A guide to methods and applications, Academic Press, Inc. New York, pp. 315–322.
Wijayawardene, N. N., Hyde, K. D., Dai, D. Q., Sanchez-Garcia, M., Goto, B. T., Saxena, R. K., Erdogdu, M., Selcuk, F., Rajeshkumar, K. C., Aptroot, A. et al. (2022): Outline of Fungi and fungus-like taxa – 2021. Mycosphere, 13(1): 53-453. doi: 10.5943/mycosphere/13/1/2
Wijayawardene, N. N., Phillips, A. J. L., Tibpromma, S., Dai, D. Q., Selbmann, L., Monteiro, J. S., Aptroot, A., Flakus, A., Rajeshkumar, K.C., Coleine, C., Pereira, D.S., Fan, X., Zhang, L., Maharachchikumbura, S.S.N., Souza, M. F., Kukwa, M., Suwannarach, N., Rodriguez-Flakus, P., Ashtekar, N., Dauner, L., Tang, L.Z., Jin, X. C. and Karunarathna, S. C. (2021): Looking for the undiscovered asexual taxa: Case studies from lesser studied life modes and habitats. Mycosphere, 12(1): 1290-1333.
Wollenzien, U., De Hoog, G. S., Krumbein, W. E. and Urzí, C. (1995): On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Science of the Total Environment, 167: 287-294.
Zalar, P., Gostinčar, C., De Hoog, G. S., Uršič, V., Sudhadham, M. and Gunde-Cimerman, N. (2008): Redefinition of Aureobasidium pullulans and its varieties. Studies in Mycology, 61: 21-38. doi: 10.3114/sim.2008.61.02
Web sources / Other sources
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