Castañar Cave is a clear example of an oligotrophic ecosystem with high hygrothermal stability both seasonal and interannual and the particularity of registering extraordinary levels of environmental radiation. These environmental conditions make the cave an ideal laboratory to evaluate both the responses of the subterranean environment to sudden changes in the matter and energy fluxes with the exterior and also any impact derived from its use as a tourist resource under a very restrictive access regime. In 2008, a fungal outbreak provoked by a vomit contaminated the sediments which were removed and subsequently treated with hydrogen peroxide. Fungal surveys were carried out in 2008 and 2009. The visits were resumed in 2014. Here, 12 years after the outbreak, we present an exhaustive study on the cave sediments in order to know the distribution of the different fungal taxa, as well as the prevalence and spatio-temporal evolution of the fungi caused by the vomit over the years under the conditions of relative isolation and high radiation that characterize this cave.

Department of Agrochemistry Environmental Microbiology and Soil Conservation Institute of Natural Resources and Agricultural Biology Seville Spain

Department of Biology and Geology University of Almeria Almeria Spain

Department of Geology Geography and Environment University of Alcala Alcala de Henares Spain

Department of Geology National Museum of Natural Sciences Madrid Spain

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology of the CAS Prague Czechia

Zobrazit více v PubMed

Abdo H., Catacchio C. R., Ventura M., D’Addabbo P., Alexandre H., Guilloux-Bénatier M., et al. . (2020). The establishment of a fungal consortium in a new winery. Sci. Rep. 10:7962. doi: 10.1038/s41598-020-64819-2, PMID: PubMed DOI PMC

Alonso-Zarza A. M., Martin-Perez A. (2008). Dolomite in caves: recent dolomite formation in oxic, non-sulfate environments. Castañar Cave, Spain. Sediment. Geol. 205, 160–164. doi: 10.1016/j.sedgeo.2008.02.006 DOI

Alonso-Zarza A. M., Martín-Pérez A., Martín-García R., Gil-Peña I., Meléndez A., Martínez-Flores E., et al. . (2011). Structural and host rock controls on the distribution, morphology and mineralogy of speleothems in the Castañar Cave (Spain). Geol. Mag. 148, 211–225. doi: 10.1017/S0016756810000506, PMID: PubMed DOI

Anitori R. P., Trott C., Saul D. J., Bergquist P. L., Walter H. R. (2002). A culture-independent survey of the bacterial community in a radon hot spring. Astrobiology 2, 255–270. doi: 10.1089/153110702762027844, PMID: PubMed DOI

Bastian F., Alabouvette C., Saiz-Jimenez C. (2009). The impact of arthropods on fungal community structure in Lascaux Cave. J. Appl. Microbiol. 106, 1456–1462. doi: 10.1111/j.1365-2672.2008.04121.x, PMID: PubMed DOI

Blachowicz A., Chiang A. J., Elsaesser A., Kalkum M., Ehrenfreund P., Stajich J. E., et al. . (2019). Proteomic and metabolomic characteristics of extremophilic fungi under simulated mars conditions. Front. Microbiol. 10:1013. doi: 10.3389/fmicb.2019.01013, PMID: PubMed DOI PMC

Bohacz J. (2017). Biodegradation of feather waste keratin by a keratinolytic soil fungus of the genus Chrysosporium and statistical optimization of feather mass loss. World J. Microbiol. Biotechnol. 33:13. doi: 10.1007/s11274-016-2177-2, PMID: PubMed DOI PMC

Bolyen E., Rideout J. R., Dillon M. R., Bokulich N. A., Abnet C., Al-Ghalith G. A., et al. . (2019). Reproducible, interactive, scalable, and extensible microbiome data science using QUIIME 2. Nat. Biotechnol. 37, 852–857. doi: 10.1038/s41587-019-0209-9, PMID: PubMed DOI PMC

Brugger J., Long N., McPhail D. C., Plimer I. (2005). An active amagmatic hydrothermal system: the Paralana hot springs, northern Flinders ranges, South Australia. Chem. Geol. 222, 35–64. doi: 10.1016/j.chemgeo.2005.06.007 DOI

Burow K., Grawunder A., Harpke M., Pietschmann S., Ehrhardt R., Wagner L., et al. . (2019). Microbiomes in an acidic rock–water cave system. FEMS Microbiol. Lett. 366:fnz167. doi: 10.1093/femsle/fnz167, PMID: PubMed DOI

Callahan B. J., Mcmurdie P. J., Rosen M. J., Han A. W., Johnson A. J., Holmes S. P. (2016). DADA2 paper supporting information: high-resolution sample inference from amplicon data. Nat. Methods 13, 581–583. doi: 10.1038/nmeth.3869, PMID: PubMed DOI PMC

Castro M. L., Barreiro F., Martínez J. J. (2011). Omphalotus olearius (DC.: Fr.) Singer: especie alóctona da micobiota de Galicia (España)? Mykes 14, 7–11.

Cigna A. A. (2005). Radon in caves. Int. J. Speleol. 34, 1–18. doi: 10.5038/1827-806X.34.1.1 DOI

Connell L. B., Rodriguez R. R., Redman R. S., Dalluge J. J. (2014). “Cold-adapted yeasts in Antarctic deserts,” in Cold-Adapted Yeasts. eds. Buzzini P., Margesin R. (Heidelberg: Springer; ), 75–98.

Connell L., Staudigel H. (2013). Fungal diversity in a dark oligotrophic volcanic ecosystem (DOVE) on mount Erebus, Antarctica. Biology 2, 798–809. doi: 10.3390/biology2020798, PMID: PubMed DOI PMC

Crous P. W., Schumacher R. K., Akulov A., Thangavel R., Hernández-Restrepo M., Carnegie A. J., et al. . (2019). New and interesting fungi. 2. Fungal Syst. Evol. 3, 57–134. doi: 10.3114/fuse.2019.03.06, PMID: PubMed DOI PMC

Cunha A. O. B., Bezerra J. D. P., Oliveira T. G. L., Barbier E., Bernard E., Machado A. R., et al. . (2020). Living in the dark: bat caves as hotspots of fungal diversity. PLoS One 15:e0243494. doi: 10.1371/journal.pone.0243494, PMID: PubMed DOI PMC

Dadachova E., Casadevall A. (2008). Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11, 525–531. doi: 10.1016/j.mib.2008.09.013, PMID: PubMed DOI PMC

Degawa Y., Gams W. (2004). A new species of Mortierella, and an associated sporangiiferous mycoparasite in a new genus, Nothadelphia. Stud. Mycol. 50, 567–572.

Dighton J., Tugay T., Zhdanova N. (2008). Fungi and ionizing radiation from radionuclides. FEMS Microbiol. Lett. 281, 109–120. doi: 10.1111/j.1574-6968.2008.01076.x PubMed DOI

Dimkić I., Stanković S., Kabić J., Stupar M., Nenadić M., Ljaljević-Grbić, et al. . (2020). Bat guano-dwelling microbes and antimicrobial properties of the pygidial gland secretion of a troglophilic ground beetle against them. Appl. Microbiol. Biotechnol. 104, 4109–4126. doi: 10.1007/s00253-020-10498-y, PMID: PubMed DOI

Dominguez-Moñino I., Jurado V., Rogerio-Candelera M. A., Hermosin B., Saiz-Jimenez C. (2021). Airborne fungi in show caves from southern Spain. Appl. Sci. 11:5027. doi: 10.3390/app11115027 PubMed DOI PMC

Domsch K. H., Gams W, Anderson T.-H. (2007). Compendium of Soil Fungi. 2nd Edn. Eching: IHW-Verlag.

Dupont J., Jacquet C., Dennetiere B., Lacoste S., Bousta F., Orial G., et al. . (2007). Invasion of the French Paleolithic painted cave of Lascaux by members of the Fusarium solani species complex. Mycologia 99, 526–533. doi: 10.1080/15572536.2007.11832546, PMID: PubMed DOI

Durrell L. W., Shields L. M. (1960). Fungi isolated in culture from soils of the Nevada test site. Mycologia 52, 636–641. doi: 10.2307/3756096 DOI

Egorova A. S., Gessler N. N., Ryasanova L. P., Kulakovskaya T. V., Belozerskaya T. A. (2015). Stress resistance mechanisms in the indicator fungi from highly radioactive Chernobyl zone sites. Microbiology 84, 152–158. doi: 10.1134/S0026261715020034 PubMed DOI

Eslyn W. E., Lombard F. F. (1983). Decay in mine timbers. Part II. Basidiomycetes associated with decay of coal mine timbers. Forest Prod. J. 33, 19–23.

Fernandez-Cortes A., Sanchez-Moral S., Cuezva S., Benavente D., Abella R. (2011). Characterization of tracer gases fluctuations on a “low energy” cave (Castañar de Ibor, Spain) using techniques of entropy of curves. Int. J. Climatol. 31, 127–143. doi: 10.1002/joc.2057 DOI

Fernandez-Cortes A., Sanchez-Moral S., Cuezva S., Cañaveras J. C., Abella R. (2009). Annual and transient signatures of gas exchange and transport in the Castañar de Ibor cave (Spain). Int. J. Speleol. 38, 153–162. doi: 10.5038/1827-806X.38.2.6 DOI

Fuma S., Ihara S., Takahashi H., Inaba O., Sato Y., Kubota Y., et al. . (2017). Radiocaesium contamination and dose rate estimation of terrestrial and freshwater wildlife in the exclusion zone of the Fukushima Dai-ichi nuclear power plant accident. J. Environ. Radioac. 171, 176–188. doi: 10.1016/j.jenvrad.2017.02.013, PMID: PubMed DOI

Garcia-Guinea J., Fernandez-Cortes A., Alvarez-Gallego M., Garcia-Antón E., Casas-Ruiz M., Blázquez-Pérez D., et al. . (2013). Leaching of uranyl–silica complexes from the host metapelite rock favoring high radon activity of subsoil air: case of Castañar cave (Spain). J. Radioanal. Nucl. Chem. 298, 1567–1585. doi: 10.1007/s10967-013-2587-7 DOI

Garzoli L., Riccucci M., Patriarca E., Debernardi P., Boggero A., Pecoraro L., et al. . (2019). First isolation of Pseudogymnoascus destructans, the fungal causative agent of white-nose disease, in bats from Italy. Mycopathologia 184, 637–644. doi: 10.1007/s11046-019-00371-6, PMID: PubMed DOI

Gessler N. N., Egorova A. S., Belozerskaya T. A. (2014). Melanin pigments of fungi under extreme environmental conditions (review). Appl. Biochem. Microbiol. 50, 105–113. doi: 10.1134/S0003683814020094 PubMed DOI

Giurgiu A., Tamas T. (2013). Mineralogical data on bat guano deposits from three Romanian caves. Studia UBB Geol. 58, 13–18. doi: 10.5038/1937-8602.58.2.2 DOI

Gomes R. R., Glienke C., Videira S. I. R., Lombard L., Groenewald J. Z., Crous P. W. (2013). Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31, 1–41. doi: 10.3767/003158513X666844, PMID: PubMed DOI PMC

Gonzalez-Menendez V., Martin J., Siles J. A., Gonzalez-Tejero M. R., Reyes F., Platas G., et al. . (2017). Biodiversity and chemotaxonomy of Preussia isolates from the Iberian Peninsula. Mycol. Prog. 16, 713–728. doi: 10.1007/s11557-017-1305-1 DOI

Held B. W., Salomon C. E., Blanchette R. A. (2020). Diverse subterranean fungi of an underground iron ore mine. PLoS One 15:e0234208. doi: 10.1371/journal.pone.0234208, PMID: PubMed DOI PMC

Heredia G., Arias-Mota R. M., Mena-Portales J., Castañeda-Ruiz R. F. (2018). Saprophytic synnematous microfungi. New records and known species for Mexico. Rev. Mex. Biodivers. 89, 604–618. doi: 10.22201/ib.20078706e.2018.3.2352 DOI

Hill C. A., Forti P. (1997). Cave Minerals of the World. 2nd Edn. Huntsville: National Speleological Society.

Holz P. H., Lumsden L. F., Marenda M. S., Browning G. F., Hufschmid J. (2018). Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLoS One 13:e0204282. doi: 10.1371/journal.pone.0204282, PMID: PubMed DOI PMC

Jiang J.-R., Cai L., Liu F. (2017). Oligotrophic fungi from a carbonate cave, with three new species of Cephalotrichum. Mycology 8, 164–177. doi: 10.1080/21501203.2017.1366370 DOI

Jurado V., Del Rosal Y., Liñan C., Martin-Pozas T., Gonzalez-Pimentel J. L., Saiz-Jimenez C. (2021). Diversity and seasonal dynamics of airborne fungi in Nerja Cave, Spain. Appl. Sci. 11:6236. doi: 10.3390/app11136236 DOI

Jurado V., Porca E., Cuezva S., Fernandez-Cortes A., Sanchez-Moral S., Saiz-Jimenez C. (2010). Fungal outbreak in a show cave. Sci. Total Environ. 408, 3632–3638. doi: 10.1016/j.scitotenv.2010.04.057 PubMed DOI

Karunarathna S. C., Dong Y., Karasaki S., Tibpromma S., Hyde K. D., Lumyong S., et al. . (2020). Discovery of novel fungal species and pathogens on bat carcasses in a cave in Yunnan Province, China. Emerg. Microbes Infect. 9, 1554–1566. doi: 10.1080/22221751.2020.1785333, PMID: PubMed DOI PMC

Khan S. R. (1998). “Phosphate urolithiasis, rat,” in Urinary System. Monographs on Pathology of Laboratory Animals. eds. Jones T. C., Hard G. C., Mohr U. (Berlin: Springer; ), 451–456.

Korhonen A., Seelan J. S. S., Miettinen O. (2018). Cryptic species diversity in polypores: the Skeletocutis nivea species complex. MycoKeys 36, 45–82. doi: 10.3897/mycokeys.36.27002, PMID: PubMed DOI PMC

Kujawska B., Rudawska M., Wilgan R., Leski T. (2021). Similarity and differences among soil fungal assemblages in managed forests and formerly managed forest reserves. Forests 12:353. doi: 10.3390/f12030353 DOI

Larcher G., Bouchara J. P., Pailley P., Montfort D., Behuin H., De Biève C., et al. . (2003). Fungal biota associated with bats in Western France. J. Med. Mycol. 13, 29–34.

Lario J., Sanchez-Moral S., Cuezva S., Taborda M., Soler V. (2006). High 222Rn levels in a show cave (Castañar de Ibor, Spain): proposal and application on management measures to minimize the effects on guides and visitors. Atmos. Environ. 40, 7395–7400. doi: 10.1016/j.atmosenv.2006.06.046 DOI

Li C.-C., Chung H.-P., Wen H.-W., Chang C.-Y., Wang Y.-T., Chou F.-I. (2015). The radiation resistance and cobalt biosorption activity of yeast strains isolated from the Lanyu low-level radioactive waste repository in Taiwan. J. Environ. Radioact. 146, 80–87. doi: 10.1016/j.jenvrad.2015.04.010, PMID: PubMed DOI

Li A.-H., Yuan F.-X., Groenewald M., Bensch K., Yurkov A. M., Li K., et al. . (2020). Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: proposal of two new orders, three new families, eight new genera and one hundred and seven new species. Stud. Mycol. 96, 17–140. doi: 10.1016/j.simyco.2020.01.002, PMID: PubMed DOI PMC

Lu X. H., Chen A. J., Zhang X. S., Jiao X. L., Gao W. W. (2014). First report of Rhexocercosporidium panacis causing rusty root of Panax ginseng in northeastern China. Plant Dis. 98:1580. doi: 10.1094/PDIS-01-14-0082-PDN, PMID: PubMed DOI

Ludwig L., Muraoka J. Y., Bonacorsi C., Donofrio F. C. (2023). Diversity of fungi obtained from bats captured in urban forest fragments in Sinop, Mato Grosso, Brazil. Braz. J. Biol. 83:e247993. doi: 10.1590/1519-6984.247993, PMID: PubMed DOI

Man B., Wang H., Yun Y., Xiang X., Wang R., Duan Y., et al. . (2018). Diversity of fungal communities in Heshang Cave of Central China revealed by mycobiome-sequencing. Front. Microbiol. 9:1400. doi: 10.3389/fmicb.2018.01400, PMID: PubMed DOI PMC

Martin-Sanchez P. M., Jurado V., Porca E., Bastian F., Lacanette D., Alabouvette C., et al. . (2014). Aerobiology of Lascaux Cave (France). Int. J. Speleol. 43, 295–303. doi: 10.5038/1827-806X.43.3.6 DOI

Mašínová T., Bahnmann B. D., Větrovský T., Tomšovský M., Merunková K., Baldrian P. (2017). Drivers of yeast community composition in the litter and soil of a temperate forest. FEMS Microbiol. Ecol. 93:fiw223. doi: 10.1093/femsec/fiw223, PMID: PubMed DOI

McMurdie P. J., Holmes S. (2013). Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. doi: 10.1371/journal.pone.0061217, PMID: PubMed DOI PMC

Nagai K., Suzuki K., Okada G. (1998). Studies on the distribution of alkalophilic and alkali-tolerant soil fungi II: fungal flora in two limestone caves in Japan. Mycoscience 39, 293–298. doi: 10.1007/BF02464011 DOI

Nguyen H. D., Nickerson N. L., Seifert K. A. (2013). Basidioascus and Geminibasidium: a new lineage of heat-resistant and xerotolerant basidiomycetes. Mycologia 105, 1231–1250. doi: 10.3852/12-351, PMID: PubMed DOI

Nováková A. (2009). Microscopic fungi isolated from the Domica cave system (Slovak karst National Park, Slovakia). A review. Int. J. Speleol. 38, 71–82. doi: 10.5038/1827-806X.38.1.8 DOI

Nováková A. (2021). Výskyt hub v jeskyních a jiných podzemních prostorách Slovenské republiky (Fungal occurrence in caves and other underground spaces in the Slovak Republic). Acta Carsologica Slovaca 59, 5–58.

Nováková A., Hubka V., Valinová S., Kolařík M., Hillebrand-Voiculescu A. M. (2018). Cultivable microscopic fungi from an underground chemosynthesis-based ecosystem: a preliminary study. Folia Microbiol. 63, 43–55. doi: 10.1007/s12223-017-0527-6, PMID: PubMed DOI

Out B., Boyle S., Cheeptham N. (2016). Identification of fungi from soil in the Nakimu caves of glacier National Park. UJEMI+ 2, 26–32.

Pagano M.C. (2016). Recent Advances on Mycorrhizal Fungi. Cham: Springer.

Péter G., Takashima M., Cadez N. (2017). “Yeast habitats: different but global,” in Yeasts in Natural Ecosystems: Ecology. eds. Buzzini P., Lachance M.-A., Yurkov A. (Cham: Springer; ), 39–71.

Popkova A. V., Mazina S. E. (2019). Microbiota of hypogean habitats in Otap Head Cave. J. Environ. Res. Eng. Manag. 75, 71–82. doi: 10.5755/j01.erem.75.3.21106 DOI

Porca E., Jurado V., Martin-Sanchez P. M., Hermosin B., Bastian F., Alabouvette C., et al. . (2011). Aerobiology: an ecological indicator for early detection and control of fungal outbreaks in caves. Ecol. Indic. 11, 1594–1598. doi: 10.1016/j.ecolind.2011.04.003 DOI

Ren H., Wang H., Yu Z., Zhang S., Qi X., Sun L., et al. . (2021). Effect of two kinds of fertilizers on growth and rhizosphere soil properties of bayberry with decline disease. Plan. Theory 10:2386. doi: 10.3390/plants10112386, PMID: PubMed DOI PMC

Romsdahl J., Blachowicz A., Chiang A. J., Singh N., Stajich J. E., Kalkum M., et al. . (2018). Characterization of Aspergillus niger Isolated from the International Space Station. mSystems 3, e00112–e00118. doi: 10.1128/mSystems.00112-18 PubMed DOI PMC

Sanchez-Moral S., Jurado V., Fernandez-Cortes A., Cuezva S., Martin-Pozas T., Gonzalez-Pimentel J. L., et al. . (2021). Environment-driven control of fungi in subterranean ecosystems: the case of La Garma cave (northern Spain). Int. Microbiol. 24, 573–591. doi: 10.1007/s10123-021-00193-x, PMID: PubMed DOI PMC

Sannino C., Borruso L., Mezzasoma A., Battistel D., Ponti S., Turchetti B., et al. . (2021). Abiotic factors affecting the bacterial and fungal diversity of permafrost in a rock glacier in the Stelvio Pass (Italian Central Alps). Appl. Soil Ecol. 166:104079. doi: 10.1016/j.apsoil.2021.104079 DOI

Saxena P., Kumar A., Shrivastava J. N. (2004). Diversity of keratinophilic mycoflora in the soil of Agra (India). Folia Microbiol. 49, 430–434. doi: 10.1007/BF02931605, PMID: PubMed DOI

Shuryak I., Matrosova V. Y., Gaidamakova E. K., Tkavc R., Grichenko O., Klimenkova P., et al. . (2017). Microbial cells can cooperate to resist high- level chronic ionizing radiation. PLoS One 12:e0189261. doi: 10.1371/journal.pone.0189261, PMID: PubMed DOI PMC

Siasou E., Johnson D., Willey N. J. (2017). An extended dose–response model for microbial responses to ionizing radiation. Front. Environ. Sci. 5:6. doi: 10.3389/fenvs.2017.00006 DOI

Somlai J., Hakl J., Kávási N., Szeiler G., Szabó P., Kovács T. (2011). Annual average radon concentration in the show caves of Hungary. J. Radioanal. Nucl. Chem. 287, 427–433. doi: 10.1007/s10967-010-0841-9 DOI

Traxler L., Wollenberg A., Steinhauser G., Chyzhevskyi I., Dubchak S., Großmann S., et al. . (2021). Survival of the basidiomycete Schizophyllum commune in soil under hostile environmental conditions in the Chernobyl exclusion zone. J. Hazard. Mater. 403:124002. doi: 10.1016/j.jhazmat.2020.124002, PMID: PubMed DOI

Turenne C. Y., Sanche S. E., Hoban D. J., Karlowsky J. A., Kabani A. M. (1999). Rapid identification of fungi by using the ITS2 genetic region and an automated fluorescent capillary electrophoresis system. J. Clin. Microbiol. 37, 1846–1851. doi: 10.1128/JCM.37.6.1846-1851.1999, PMID: PubMed DOI PMC

Ulloa M., Lappe P., Aguilar S., Park H., Pérez-Mejía A., Toriello C., et al. . (2006). Contribution to the study of the mycobiota present in the natural habitats of Histoplasma capsulatum: an integrative study in Guerrero, Mexico. Rev. Mex. Biodivers. 77, 153–168.

UNITE Community (2019). UNITE QIIME release for fungi. Version 18.11.2018. 10.15156/BIO/786334.

Urbaniak C., van Dam P., Zaborin A., Zaborina O., Gilbert J. A., Torok T., et al. . (2019). Genomic characterization and virulence potential of two Fusarium oxysporum isolates cultured from the International Space Station. mSystems 4, e00345–e00318. doi: 10.1128/mSystems.00345-18 PubMed DOI PMC

Van Houdt R., Mijnendonckx K., Leys N. (2012). Microbial contamination monitoring and control during human space missions. Planet. Space Sci. 60, 115–120. doi: 10.1016/j.pss.2011.09.001 DOI

Vanam H. P., Rao P. N., Mohanran K., Yegneswaran P. P., Rudramurthy S. P. M. (2018). Distal lateral subungual onychomycosis owing to Tritirachium oryzae: A bystander or invader? Mycopathologia 183, 459–463. doi: 10.1007/s11046-017-0226-5 PubMed DOI

Vanderwolf K. J., Malloch D., McAlpine D. F. (2019). No change detected in culturable fungal assemblages on cave walls in eastern Canada with the introduction of Pseudogymnoascus destructans. Diversity 11:222. doi: 10.3390/d11120222 DOI

Wagner L., Stielow B., Hoffmann K., Petkovits T., Papp T., Vágvölgyi C., et al. . (2011). Molecular characterization of airborne fungi in caves of the Mogao grottoes, Dunhuang, China. Int. Biodeter. Biodegr. 65, 726–731. doi: 10.1016/j.ibiod.2011.04.006 DOI

Wang Q.-M., Yurkov A. M., Göker M., Lumbsch H. T., Leavitt S. D., Groenewald M., et al. . (2016). Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud. Mycol. 81, 149–189. doi: 10.1016/j.simyco.2015.12.002 PubMed DOI PMC

Wasti I. G., Fui F. S., Zhi T. Q., Mun C. W., Kassim M. H. S., Dawood M. M., et al. . (2020). Fungi from dead arthropods and bats of Gomantong cave, northern Borneo, Sabah (Malaysia). J. Cave Karst Stud. 82, 261–275. doi: 10.4311/2019MB0146 DOI

Weidler G. W., Dornmayr-Pfaffenhuemer M., Gerbl F. W., Heinen W., Stan-Lotter H. (2007). Communities of archaea and bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota. Appl. Environ. Microbiol. 73, 259–270. doi: 10.1128/AEM.01570-06, PMID: PubMed DOI PMC

White T. J., Bruns T., Lee S., Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR Protocols: A Guide to Methods and Applications. eds. Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. (London: Academic Press; ), 315–322.

Zhang Z. F., Liu F., Zhou X., Liu X. Z., Liu S. J., Cai L. (2017). Culturable mycobiota from karst caves in China, with descriptions of 20 new species. Persoonia 39, 1–31. doi: 10.3767/persoonia.2017.39.01, PMID: PubMed DOI PMC

Zhang T., Victor T. R., Rajkumar S. S., Li X., Okoniewski J. C., Hicks A. C., et al. . (2014). Mycobiome of the bat white nose syndrome affected caves and mines reveals diversity of fungi and local adaptation by the fungal pathogen Pseudogymnoascus (Geomyces) destructans. PLoS One 9:e108714. doi: 10.1371/journal.pone.0108714, PMID: PubMed DOI PMC

Zhdanova N. N., Vasilevskaya A. I., Lashko T. N., Gavrilyuk V. I., Dighton J. (1994). Changes in micromycetes communities in soil in response to pollution by long-lived radionuclides emitted in the Chernobyl accident. Mycol. Res. 98, 789–795. doi: 10.1016/S0953-7562(09)81057-5 DOI

Zhdanova N. N., Zakharchenko V. A., Vember V. V., Nakonechnaya L. T. (2000). Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol. Res. 104, 1421–1426. doi: 10.1017/S0953756200002756 DOI

Zheng H., Blechert O., Mei H., Ge L., Liu J., Tao Y., et al. . (2020). Assembly and analysis of the whole genome of Arthroderma uncinatum strain T10, compared with Microsporum canis and Trichophyton rubrum. Mycoses 63, 683–693. doi: 10.1111/myc.13079, PMID: PubMed DOI

A Second Fungal Outbreak in Castañar Cave, Spain, Discloses the Fragility of Subsurface Ecosystems