Niches and Adaptations of Polyextremotolerant Black Fungi

  • Martin Grube
  • Lucia Muggia
  • Cene Gostinčar
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 27)


Environmental changes such as increased levels of carbon dioxide and UV radiation are usually perceived as a threat to living organisms and associated with shrinking populations and extinction. We frequently forget that some species cope really well with a range of extreme and rapidly changing conditions and may actually benefit from such changes. Black meristematic fungi, for example, are well adapted to high doses of radiation and survive long periods of desiccation. They seem not only robust under moderate stress conditions but seem to adapt and diversify, in agreement with the so-called concept of antifragility. We hypothesise that this behaviour is mediated by the polymer melanin in the cell walls; yet, other protective molecules and phenotypic plasticity play an important role as well. Evolution of these fungi is thought to have originated in the harsh oligotrophic habitats on the surface and subsurface of rocks, but their potentials are much wider than that. Their polyextremotolerance helps them to colonise numerous habitats in which competition with other fungi is low due to stressful conditions. This includes a range of anthropogenic environments and in some cases also animal bodies. Some of these fungi also undergo lichen-like associations with photoautotrophs or benefit from growing on lichens.


Aureobasidium Pullulans Splenic Abscess Protective Compound Black Fungus Lichen Symbiosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



LM and MG are grateful to the Austrian Science Foundation for financial support (FWF P24114). CG acknowledges the support of the project ‘Centre of excellence for integrated approaches in chemistry and biology of proteins’ number OP13., financed by the European regional development fund (85 % share of financing) and by the Slovenian Ministry of Higher Education, Science and Technology (15 % share of financing) and of the Slovenian state budget through the Slovenian Research Agency (Infrastructural Centre Mycosmo).


  1. Andrews JH, Spear RN, Nordheim EV (2002) Population biology of Aureobasidium pullulans on apple leaf surfaces. Can J Microbiol 48:500–513PubMedCrossRefGoogle Scholar
  2. Badali H, Prenafeta-Boldu FX, Guarro J, Klaassen CH, Meis JF, De Hoog GS (2011) Cladophialophora psammophila, a novel species of Chaetothyriales with a potential use in the bioremediation of volatile aromatic hydrocarbons. Fungal Biol 115:1019–1029PubMedCrossRefGoogle Scholar
  3. Bar-Even A, Noor E, Milo R (2012) A survey of carbon fixation pathways through a quantitative lens. J Exp Bot 63:2325–2342PubMedCrossRefGoogle Scholar
  4. Beumer RR, Kusumaningrum H (2003) Kitchen hygiene in daily life. Int Biodeterior Biodegrad 51:299–302CrossRefGoogle Scholar
  5. Bevilacqua A, Corbo MR, Sinigaglia M (2012) Selection of yeasts as starter cultures for table olives: a step-by-step procedure. Front Microbiol 3:194PubMedCrossRefGoogle Scholar
  6. Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212PubMedCrossRefGoogle Scholar
  7. Boustie J, Tomasi S, Grube M (2011) Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem Rev 10:287–307CrossRefGoogle Scholar
  8. Brunauer G, Blaha J, Hager A, Turk R, Stocker-Worgotter E, Grube M (2007) An isolated lichenicolous fungus forms lichenoid structures when co-cultured with various coccoid algae. Symbiosis 44:127–136Google Scholar
  9. Bryan R, Jiang ZW, Friedman M, Dadachova E (2011) The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melanization. Fungal Biol 115:945–949PubMedCrossRefGoogle Scholar
  10. Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136CrossRefGoogle Scholar
  11. Cappitelli F, Sorlini C (2008) Microorganisms attack synthetic polymers in items representing our cultural heritage. Appl Environ Microbiol 74:564–569PubMedCrossRefGoogle Scholar
  12. Casadevall A (2007) Determinants of virulence in the pathogenic fungi. Fungal Biol Rev 21:130–132PubMedCrossRefGoogle Scholar
  13. Chan GF, Puad MSA, Chin CF, Rashid NAA (2011) Emergence of Aureobasidium pullulans as human fungal pathogen and molecular assay for future medical diagnosis. Folia Microbiol (Praha) 56:459–467CrossRefGoogle Scholar
  14. Chi Z, Wang F, Yue L, Liu G, Zhang T (2009) Bioproducts from Aureobasidium pullulans, a biotechnologically important yeast. Appl Microbiol Biotechnol 82:793–804PubMedCrossRefGoogle Scholar
  15. Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11:525–531PubMedCrossRefGoogle Scholar
  16. Dadachova E, Bryan RA, Huang X, Moadel T, Schweitzer AD, Aisen P, Nosanchuk JD, Casadevall A (2007) Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS One 2:e457PubMedCrossRefGoogle Scholar
  17. Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair 11:12–21PubMedCrossRefGoogle Scholar
  18. Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 5:e12570PubMedCrossRefGoogle Scholar
  19. Danchin A, Binder P, Noria S (2011) Antifragility and tinkering in biology (and in business): flexibility provides an efficient epigenetic way to manage risk. Genes 2011:998–1016CrossRefGoogle Scholar
  20. de Felice DV, Solfrizzo M, De Curtis F, Lima G, Visconti A, Castoria R (2008) Strains of Aureobasidium pullulans can lower ochratoxin A contamination in wine grapes. Phytopathology 98:1261–1270PubMedCrossRefGoogle Scholar
  21. de Hoog GS, Guarro J, Gené F, Figueras MJ (2000) Atlas of clinical fungi, 2nd edn. Centraalbureau voor Schimmelcultures/Universitat Rovira i Virgili, Utrecht/Reus, 1126 ppGoogle Scholar
  22. de Hoog GS, Zalar P, Gerrits van den Ende AHG, Gunde-Cimerman N (2005) Relation of halotolerance to human-pathogenicity in the fungal tree of life: an overview of ecology and evolution under stress. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya. Springer, Dordrecht, pp 371–395CrossRefGoogle Scholar
  23. de Hoog GS, Zeng JS, Harrak MJ, Sutton DA (2006) Exophiala xenobiotica sp. nov., an opportunistic black yeast inhabiting environments rich in hydrocarbons. Antonie van Leeuwenhoek 90:257–268PubMedCrossRefGoogle Scholar
  24. Feazel LM, Baumgartner LK, Peterson KL, Frank DN, Harris JK, Pace NR (2009) Opportunistic pathogens enriched in showerhead biofilms. Proc Natl Acad Sci U S A 106:16393–16398PubMedCrossRefGoogle Scholar
  25. Friedl T, Büdel B (2008) Photobionts. In: Nash TH (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 9–26CrossRefGoogle Scholar
  26. Fuchs G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu Rev Microbiol 65:631–658PubMedCrossRefGoogle Scholar
  27. Fürst HM (2000) Ökologie des Hyphenpilzes Hormoconis resinae und Eigenschaften seines n-Alkan-induzierten P450-Monooxygenasesystems. Dissertation, Technische Universität Berlin, 124 pp. ISBN: 3-89825-042-3Google Scholar
  28. Gadd GM, Derome L (1988) Biosorption of copper by fungal melanin. Appl Microbiol Biotechnol 29:610–617CrossRefGoogle Scholar
  29. Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450PubMedCrossRefGoogle Scholar
  30. Gorbushina AA, Whitehead K, Dornieden T, Niesse A, Schulte A, Hedges J (2003) Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock dwelling microcolonial fungi. Can J Bot 2:131–138CrossRefGoogle Scholar
  31. Gorbushina AA, Beck A, Schulte A (2005) Microcolonial rock inhabiting fungi and lichen photo­bionts: evidence for mutualistic interactions. Mycol Res 109:1288–1296PubMedCrossRefGoogle Scholar
  32. Gostinčar C, Grube M, de Hoog GS, Zalar P, Gunde-Cimerman N (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11PubMedCrossRefGoogle Scholar
  33. Gostinčar C, Grube M, Gunde-Cimerman N (2011) Evolution of fungal pathogens in domestic environments? Fungal Biol 115:1008–1018PubMedCrossRefGoogle Scholar
  34. Grube M, Schmid F, Berg G (2011) Black fungi and associated bacterial communities in the phyllosphere of grapevine. Fungal Biol 115:978–986PubMedCrossRefGoogle Scholar
  35. Gueidan C, Villasenor CR, de Hoog GS, Gorbushina AA, Untereiner WA, Lutzoni F (2008) A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol 61:111–119PubMedCrossRefGoogle Scholar
  36. Gueidan C, Ruibal C, de Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol 115:987–996PubMedCrossRefGoogle Scholar
  37. Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitaš A (2000) Hypersaline waters in salterns – natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240Google Scholar
  38. Harutyunyan S, Muggia L, Grube M (2008) Black fungi in lichens from seasonally arid habitats. Stud Mycol 61:83–90PubMedCrossRefGoogle Scholar
  39. Hawkes M, Rennie R, Sand C, Vaudry W (2005) Aureobasidium pullulans infection: fungemia in an infant and a review of human cases. Diagn Microbiol Infect Dis 51:209–213PubMedCrossRefGoogle Scholar
  40. Henssen A (1987) Lichenothelia, a genus of microfungi on rocks. Biblioth Lichenol 25:257–293Google Scholar
  41. Huang YT, Liao CH, Huang YT, Liaw SJ, Yang JL, Lai DM, Lee YC, Hsueh PR (2008) Catheter-related septicemia due to Aureobasidium pullulans. Int J Infect Dis 12:E137–E139PubMedCrossRefGoogle Scholar
  42. Ivarson KC, Morita H (1982) Single-cell protein-production by the acid-tolerant fungus Scytalidium acidophilum from acid hydrolysates of waste paper. Appl Environ Microbiol 43:643–647PubMedGoogle Scholar
  43. Jürgensen CW, Jacobsen NR, Emri T, Eriksen SH, Pocsi I (2001) Glutathione metabolism and dimorphism in Aureobasidium pullulans. J Basic Microbiol 41:131–137PubMedCrossRefGoogle Scholar
  44. Kaarakainen P, Rintala H, Vepsalainen A, Hyvarinen A, Nevalainen A, Meklin T (2009) Microbial content of house dust samples determined with qPCR. Sci Total Environ 407:4673–4680PubMedCrossRefGoogle Scholar
  45. Kogej T, Gostinčar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N (2006) Mycosporines in extremophilic fungi – novel complementary osmolytes? Environ Chem 3:105–110CrossRefGoogle Scholar
  46. Kohlmeyer J, Hawksworth DL, Volkmann-Kohlmeyer B (2004) Observations on two “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol Prog 3:51–56CrossRefGoogle Scholar
  47. Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci U S A 102:3141–3146PubMedCrossRefGoogle Scholar
  48. Lapinskas PJ, Cunningham KW, Liu XF, Fink GR, Culotta C (1995) Mutations in Pmr1 suppress oxidative damage in yeast-cells lacking superoxide-dismutase. Mol Cell Biol 15:1382–1388PubMedGoogle Scholar
  49. Lian X, de Hoog GS (2010) Indoor wet cells harbour melanized agents of cutaneous infection. Med Mycol 48:622–628PubMedCrossRefGoogle Scholar
  50. Madhour A, Anke H, Mucci A, Davoli P, Weber RWS (2005) Biosynthesis of the xanthophyll plectaniaxanthin as a stress response in the red yeast Dioszegia (Tremellales, Heterobasidiomycetes, Fungi). Phytochemistry 66:2617–2626PubMedCrossRefGoogle Scholar
  51. Martin-Sanchez PM, Novakova A, Bastian F, Alabouvette C, Saiz-Jimeneza C (2012) Two new species of the genus Ochroconis, O. lascauxensis and O. anomala isolated from black stains in Lascaux Cave, France. Fungal Biol 116:574–589PubMedCrossRefGoogle Scholar
  52. Muggia L, Hafellner J, Wirtz N, Hawksworth DL, Grube M (2008) The sterile microfilamentous lichenized fungi Cystocoleus ebeneus and Racodium rupestre are relatives of plant pathogens and clinically important dothidealean fungi. Mycol Res 112:50–56PubMedCrossRefGoogle Scholar
  53. Nelsen MP, Lucking R, Grube M, Mbatchou JS, Muggia L, Plata ER, Lumbsch HT (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol 64:135–144PubMedCrossRefGoogle Scholar
  54. Nevo E (2001) Evolution of genome-phenome diversity under environmental stress. Proc Natl Acad Sci U S A 98:6233–6240PubMedCrossRefGoogle Scholar
  55. Nishiuchi Y, Tamaru A, Kitada S, Taguri T, Matsumoto S, Tateishi Y, Yoshimura M, Ozeki Y, Matsumura N, Ogura H, Maekura R (2009) Mycobacterium avium complex organisms predominantly colonize in the bathtub inlets of patients’ bathrooms. Jpn J Infect Dis 62:182–186PubMedGoogle Scholar
  56. Nisiotou AA, Chorianopoulos N, Nychas GJE, Panagou EZ (2010) Yeast heterogeneity during spontaneous fermentation of black Conservolea olives in different brine solutions. J Appl Microbiol 108:396–405PubMedCrossRefGoogle Scholar
  57. Ojima M, Toshima Y, Koya E, Ara K, Tokuda H, Kawai S, Kasuga F, Ueda N (2002) Hygiene measures considering actual distributions of microorganisms in Japanese households. J Appl Microbiol 93:800–809PubMedCrossRefGoogle Scholar
  58. Olstorpe M, Schnurer J, Passoth V (2010) Microbial changes during storage of moist crimped cereal barley grain under Swedish farm conditions. Anim Feed Sci Technol 156:37–46CrossRefGoogle Scholar
  59. Onofri S, Seltimann L, de Hoog GS, Grube M, Barreca D, Ruisi S, Zucconi L (2007) Evolution and adaptation of fungi at boundaries of life. Adv Space Res 40:1657–1664CrossRefGoogle Scholar
  60. Onofri S, Barreca D, Selbmann L, Isola D, Rabbow E, Horneck G, de Vera JP, Hatton J, Zucconi L (2008) Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions. Stud Mycol 61:99–109PubMedCrossRefGoogle Scholar
  61. Orell A, Navarro CA, Rivero M, Aguilar JS, Jerez CA (2012) Inorganic polyphosphates in extremophiles and their possible functions. Extremophiles 16:573–583PubMedCrossRefGoogle Scholar
  62. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10PubMedCrossRefGoogle Scholar
  63. Palmer RJ Jr, Friedmann EI (1988) Incorporation of inorganic carbon by Antarctic cryptoendolithic fungi. Polarforschung 58:189–191PubMedGoogle Scholar
  64. Prenafeta-Boldu FX, Summerbell R, de Hoog GS (2006) Fungi growing on aromatic hydrocarbons: biotechnology’s unexpected encounter with biohazard? FEMS Microbiol Rev 30:109–130PubMedCrossRefGoogle Scholar
  65. Prenafeta-Boldu FX, Guivernau M, Gallastegui G, Vinas M, de Hoog GS, Elias A (2012) Fungal/bacterial interactions during the biodegradation of TEX hydrocarbons (toluene, ethylbenzene and p-xylene) in gas biofilters operated under xerophilic conditions. FEMS Microbiol Ecol 80:722–734PubMedCrossRefGoogle Scholar
  66. Rauch ME, Graef HW, Rozenzhak SM, Jones SE, Bleckmann CA, Kruger RL, Naik RR, Stone MO (2006) Characterization of microbial contamination in United States Air Force aviation fuel tanks. J Ind Microbiol Biotechnol 33:29–36PubMedCrossRefGoogle Scholar
  67. Robert V, Stegehuis G, Stalpers J (2005) The MycoBank engine and related databases.
  68. Robiglio A, Sosa MC, Lutz MC, Lopes CA, Sangorrin MP (2011) Yeast biocontrol of fungal spoilage of pears stored at low temperature. Int J Food Microbiol 147:211–216PubMedCrossRefGoogle Scholar
  69. Ruibal C, Gueidan C, Selbmann L, Gorbushina AA, Crous PW, Groenewald JZ, Muggia L, Grube M, Isola D, Schoch CL, Staley JT, Lutzoni F, de Hoog GS (2009) Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol 64:123–133PubMedCrossRefGoogle Scholar
  70. Sailer MF, van Nieuwenhuijzen EJ, Knol W (2010) Forming of a functional biofilm on wood surfaces. Ecol Eng 36:163–167CrossRefGoogle Scholar
  71. Schlichting CD (2008) Hidden reaction norms, cryptic genetic variation, and evolvability. Ann N Y Acad Sci 1133:187–203PubMedCrossRefGoogle Scholar
  72. Scott JA, Untereiner WA, Ewaze JO, Wong B, Doyle D (2007) Baudoinia, a new genus to accommodate Torula compniacensis. Mycologia 99:592–601PubMedCrossRefGoogle Scholar
  73. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51:1–32Google Scholar
  74. Selbmann L, de Hoog GS, Zucconi L, Isola D, Ruisi S, van den Ende AHGG, Ruibal C, De Leo F, Urzi C, Onofri S (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol 61:1–20PubMedCrossRefGoogle Scholar
  75. Seyedmousavi S, Badali H, Chlebicki A, Zhao JJ, Prenafeta-Boldu FX, De Hoog GS (2011) Exophiala sideris, a novel black yeast isolated from environments polluted with toxic alkyl benzenes and arsenic. Fungal Biol 115:1030–1037PubMedCrossRefGoogle Scholar
  76. Shah AA, Hasan F, Hameed A, Ahmed S (2008) Biological degradation of plastics: a comprehensive review. Biotechnol Adv 26:246–265PubMedCrossRefGoogle Scholar
  77. Shima J, Takagi H (2009) Stress-tolerance of baker’s-yeast (Saccharomyces cerevisiae) cells: stress-protective molecules and genes involved in stress tolerance. Biotechnol Appl Biochem 53:155–164PubMedCrossRefGoogle Scholar
  78. Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101:823–832PubMedCrossRefGoogle Scholar
  79. Sterflinger K, Tesei D, Zakharova K (2012) Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecol 5:453–462CrossRefGoogle Scholar
  80. Su HJ, Rotnitzky A, Burge HA, Spengler JD (1992) Examination of fungi in domestic interiors by using factor-analysis – correlations and associations with home factors. Appl Environ Microbiol 58:181–186PubMedGoogle Scholar
  81. Summerbell RC, Staib F, Dales R, Nolard N, Kane J, Zwanenburg H, Burnett R, Krajden S, Fung D, Leong D (1992) Ecology of fungi in human dwellings. J Med Vet Mycol 30:279–285PubMedCrossRefGoogle Scholar
  82. Takagi H (2008) Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl Microbiol Biotechnol 81:211–223PubMedCrossRefGoogle Scholar
  83. Taleb NN (2011) Antifragility – or – the property of disorder-loving systems. Edge. Available online: Accessed on 2 Aug 2012
  84. Turick CE, Ekechukwu AA, Milliken CE, Casadevall A, Dadachova E (2011) Gamma radiation interacts with melanin to alter its oxidation-reduction potential and results in electric current production. Bioelectrochemistry 82:69–73PubMedCrossRefGoogle Scholar
  85. Vadkertiova R, Slavikova E (1995) Killer activity of yeasts isolated from the water environment. Can J Microbiol 41:759–766PubMedCrossRefGoogle Scholar
  86. Webb JS, Nixon M, Eastwood IM, Greenhalgh M, Robson GD, Handley PS (2000) Fungal colonization and biodeterioration of plasticized polyvinyl chloride. Appl Environ Microbiol 66:3194–3200PubMedCrossRefGoogle Scholar
  87. West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102:6543–6549PubMedCrossRefGoogle Scholar
  88. Zalar P, de Hoog GS, Schroers HJ, Crous PW, Groenewald JZ, Gunde-Cimerman N (2007) Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Stud Mycol 58:157–183PubMedCrossRefGoogle Scholar
  89. Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 61:21–38PubMedCrossRefGoogle Scholar
  90. Zalar P, Novak M, De Hoog GS, Gunde-Cimerman N (2011) Dishwashers – a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol 115:997–1007PubMedCrossRefGoogle Scholar
  91. Zhao JJ, Zeng JS, de Hoog GS, Attili-Angelis D, Prenafeta-Boldu FX (2010) Isolation and identification of black yeasts by enrichment on atmospheres of monoaromatic hydrocarbons. Microb Ecol 60:149–156PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of Plant SciencesKarl-Franzens-University GrazGrazAustria
  2. 2.Department of Biology, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  3. 3.Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP)LjubljanaSlovenia
  4. 4.Department of Life ScienceUniversity of TriesteTriesteItaly

Personalised recommendations