Black yeast

“Black yeasts”, sometimes also black fungi, dematiaceous fungi, microcolonial fungi or meristematic fungi[1] is a diverse group of slow-growing microfungi which reproduce mostly asexually (fungi imperfecti). Only few genera reproduce by budding cells, while in others hyphal or meristematic (isodiametric) reproduction is preponderant.[2][3][4][5] Black yeasts share some distinctive characteristics, in particular melanisation of their cell wall. Morphological plasticity, incrustation of the cell wall with melanins and presence of other protective substances like carotenoids and mycosporines[6] represent passive physiological adaptations which enable black fungi to be highly resistant against environmental stresses.[7] The term "polyextremotolerance" has been introduced to describe this phenotype, a good example of which is the species Aureobasidium pullulans.[8] Presence of 1,8-dihydroxynaphtalene melanin in the cell wall[9] confers to the microfungi their characteristic olivaceous to dark brown/black colour.

The consortium comprises two phylogenetically very different fungal groups.[10][11] Many are found in the orders Capnodiales, Dothideales, and Pleosporales (class Dothideomycetes). These black fungi mostly have an extremotolerant life style. Many representatives of this group can colonize bare rocks e.g. in the Mediterranean basin or in hot and cold dry deserts and are therefore referred to as rock-inhabiting fungi,[10][11] or occur in salterns.[12] These black yeasts are believed to be the most resistant eukaryotic organisms known to-date.[7] They were firstly described in the early 80s by three almost concomitant seminal research articles.[13][14][15] Members of Chaetothyriales (class Eurotiomycetes)[10][11] are found in hydrocarbon-rich environments or in nutrient poor, moist indoor environments, and may occur as opportunistic pathogens of vertebrate hosts, such as Exophiala (Wangiella) dermatitidis.[16] Several species are associated with lichens[17][18] as well as other phototrophs[19] and sometimes with ants in specific ant-fungi associations.[20]

In recent years, black fungi such as E. dermatitidis or Hortaea werneckii have attracted increasingly attention as model microorganisms in studies on astrobiology,[21] bioremediation of polluted ecosystems by biofiltration,[22] effect of ionizing radiations in contaminated area,[23][24] biodeterioration of materials,[25][26] and mechanisms of adaptation to high salt concentrations.[12] A collaborative effort coordinated by the Broad Institute is currently ongoing to sequence the genomes of several black fungi to shed light into their ecology, phylogeny and pathogenicity.

In 2011, a research paper about occurrence of potentially pathogenic black fungi in household dishwashers[27] was partially misreported by the media and went viral.

Black yeasts are not related to the edible cloud ear fungus Auricularia polytricha.[10][11]

References

  1. Sterflinger, Katja (2006). "Black Yeasts and Meristematic Fungi: Ecology, Diversity and Identification". In Rosa, Carlos; Gábor, Péter. Biodiversity and Ecophysiology of Yeasts. The Yeast Handbook. pp. 501–14. doi:10.1007/3-540-30985-3_20. ISBN 3-540-26100-1.
  2. Sudhadham, M.; Prakitsin, S.; Sivichai, S.; Chaiyarat, R.; Dorrestein, G. M.; Menken, S.B.J.; De Hoog, G.S. (2008). "The neurotropic black yeast Exophiala dermatitidis has a possible origin in the tropical rain forest". Studies in Mycology. 61: 145–55. doi:10.3114/sim.2008.61.15. PMC 2610309Freely accessible. PMID 19287537.
  3. de Hoog, GS; Hermanides-Nijhof, EJ (1977). "The Black Yeasts and Allied Hyphomycetes". Studies in Mycology. 15: 1–222. OCLC 222951121.
  4. Butinar, Lorena; Sonjak, Silva; Zalar, Polona; Plemenitaš, Ana; Gunde-Cimerman, Nina (2005). "Melanized halophilic fungi are eukaryotic members of microbial communities in hypersaline waters of solar salterns". Botanica Marina. 48. doi:10.1515/BOT.2005.007.
  5. Matos, T; De Hoog, GS; De Boer, AG; De Crom, I; Haase, G (2002). "High prevalence of the neurotrope Exophiala dermatitidis and related oligotrophic black yeasts in sauna facilities". Mycoses. 45 (9–10): 373–7. doi:10.1046/j.1439-0507.2002.00779.x. PMID 12421284.
  6. Gorbushina, A.A.; Kotlova, E.R.; Sherstneva, O.A. (2008). "Cellular responses of microcolonial rock fungi to long-term desiccation and subsequent rehydration". Studies in Mycology. 61: 91–7. doi:10.3114/sim.2008.61.09. PMC 2610304Freely accessible. PMID 19287531.
  7. 1 2 Gostinčar, Cene; Grube, Martin; De Hoog, Sybren; Zalar, Polona; Gunde-Cimerman, Nina (2010). "Extremotolerance in fungi: Evolution on the edge". FEMS Microbiology Ecology. 71 (1): 2–11. doi:10.1111/j.1574-6941.2009.00794.x. PMID 19878320.
  8. Gostinčar, C.; Grube, M.; Gunde-Cimerman, N. (2011). "Evolution of Fungal Pathogens in Domestic Environments?". Fungal Biology. 115 (10): 1008–1018. doi:10.1016/j.funbio.2011.03.004. PMID 21944213.
  9. Kogej, Tina; Wheeler, Michael H; Lanišnik Rižner, Tea; Gunde-Cimerman, Nina (2004). "Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions". FEMS Microbiology Letters. 232 (2): 203–9. doi:10.1016/S0378-1097(04)00073-4. PMID 15033240.
  10. 1 2 3 4 Gueidan, C.; Villasenor, C. R.; De Hoog, G. S.; Gorbushina, A. A.; Untereiner, W. A.; Lutzoni, F. (2008). "A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages". Studies in Mycology. 61: 111–9. doi:10.3114/sim.2008.61.11. PMC 2610302Freely accessible. PMID 19287533.
  11. 1 2 3 4 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.; De Hoog, G.S. (2010). "Phylogeny of rock-inhabiting fungi related to Dothideomycetes". Studies in Mycology. 64: 123–133S7. doi:10.3114/sim.2009.64.06. PMC 2816969Freely accessible. PMID 20169026.
  12. 1 2 Plemenitaš, A.; Vaupotič, T.; Lenassi, M.; Kogej, T.; Gunde-Cimerman, N. (2008). "Adaptation of extremely halotolerant black yeast Hortaea werneckii to increased osmolarity: A molecular perspective at a glance". Studies in Mycology. 61: 67–75. doi:10.3114/sim.2008.61.06. PMC 2610308Freely accessible. PMID 19287528.
  13. Staley, J. T.; Palmer, F.; Adams, J. B. (1982). "Microcolonial Fungi: Common Inhabitants on Desert Rocks?". Science. 215 (4536): 1093–5. doi:10.1126/science.215.4536.1093. PMID 17771840.
  14. Krumbein, W. E.; Jens, K. (1981). "Biogenic rock varnishes of the negev desert (Israel) an ecological study of iron and manganese transformation by cyanobacteria and fungi". Oecologia. 50: 25–38. doi:10.1007/BF00378791.
  15. Friedmann, E. I. (1982). "Endolithic Microorganisms in the Antarctic Cold Desert". Science. 215 (4536): 1045–53. doi:10.1126/science.215.4536.1045. PMID 17771821.
  16. De Hoog GS, Guarro J, Gené J, Figueras MJ (2009). Atlas of Clinical Fungi, third ed. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands.
  17. Muggia, Lucia; Gueidan, Cecile; Knudsen, Kerry; Perlmutter, Gary; Grube, Martin (2012). "The Lichen Connections of Black Fungi". Mycopathologia. 175 (5–6): 523–35. doi:10.1007/s11046-012-9598-8. PMID 23161018.
  18. Harutyunyan, S.; Muggia, L.; Grube, M. (2008). "Black fungi in lichens from seasonally arid habitats". Studies in Mycology. 61: 83–90. doi:10.3114/sim.2008.61.08. PMC 2610299Freely accessible. PMID 19287530.
  19. Gostinčar, Cene; Muggia, Lucia; Grube, Martin (2012). "Polyextremotolerant black fungi: Oligotrophism, adaptive potential, and a link to lichen symbioses". Frontiers in Microbiology. 3. doi:10.3389/fmicb.2012.00390.
  20. Voglmayr, Hermann; Mayer, Veronika; Maschwitz, Ulrich; Moog, Joachim; Djieto-Lordon, Champlain; Blatrix, Rumsaïs (2011). "The diversity of ant-associated black yeasts: Insights into a newly discovered world of symbiotic interactions". Fungal Biology. 115 (10): 1077–91. doi:10.1016/j.funbio.2010.11.006. PMID 21944219.
  21. Onofri, S.; Barreca, D.; Selbmann, L.; Isola, D.; Rabbow, E.; Horneck, G.; De Vera, J.P.P.; Hatton, J.; Zucconi, L. (2008). "Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions". Studies in Mycology. 61: 99–109. doi:10.3114/sim.2008.61.10. PMC 2610303Freely accessible. PMID 19287532.
  22. Prenafeta-Boldú, Francesc X.; Summerbell, Richard; Sybren De Hoog, G. (2006). "Fungi growing on aromatic hydrocarbons: Biotechnology's unexpected encounter with biohazard?". FEMS Microbiology Reviews. 30 (1): 109–30. doi:10.1111/j.1574-6976.2005.00007.x. PMID 16438682.
  23. Robertson, Kelly L.; Mostaghim, Anahita; Cuomo, Christina A.; Soto, Carissa M.; Lebedev, Nikolai; Bailey, Robert F.; Wang, Zheng (2012). Nielsen, Kirsten, ed. "Adaptation of the Black Yeast Wangiella dermatitidis to Ionizing Radiation: Molecular and Cellular Mechanisms". PLoS ONE. 7 (11): e48674. doi:10.1371/journal.pone.0048674. PMC 3490873Freely accessible. PMID 23139812.
  24. Dadachova, Ekaterina; Bryan, Ruth A.; Huang, Xianchun; Moadel, Tiffany; Schweitzer, Andrew D.; Aisen, Philip; Nosanchuk, Joshua D.; Casadevall, Arturo (2007). Rutherford, Julian, ed. "Ionizing Radiation Changes the Electronic Properties of Melanin and Enhances the Growth of Melanized Fungi". PLoS ONE. 2 (5): e457. doi:10.1371/journal.pone.0000457. PMC 1866175Freely accessible. PMID 17520016.
  25. Cappitelli, F.; Nosanchuk, J. D.; Casadevall, A.; Toniolo, L.; Brusetti, L.; Florio, S.; Principi, P.; Borin, S.; Sorlini, C. (2006). "Synthetic Consolidants Attacked by Melanin-Producing Fungi: Case Study of the Biodeterioration of Milan (Italy) Cathedral Marble Treated with Acrylics". Applied and Environmental Microbiology. 73 (1): 271–7. doi:10.1128/AEM.02220-06. PMC 1797126Freely accessible. PMID 17071788.
  26. Gorbushina, A. A.; Krumbein, W. E.; Hamman, C. H.; Panina, L.; Soukharjevski, S.; Wollenzien, U. (1993). "Role of black fungi in color change and biodeterioration of antique marbles". Geomicrobiology Journal. 11 (3–4): 205–221. doi:10.1080/01490459309377952.
  27. Zalar, P.; Novak, M.; De Hoog, G.S.; Gunde-Cimerman, N. (2011). "Dishwashers – A man-made ecological niche accommodating human opportunistic fungal pathogens". Fungal Biology. 115 (10): 997–1007. doi:10.1016/j.funbio.2011.04.007. PMID 21944212. Lay summary ScienceDaily (June 20, 2011).

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