1932

Abstract

Hypersaline waters and glacial ice are inhospitable environments that have low water activity and high concentrations of osmolytes. They are inhabited by diverse microbial communities, of which extremotolerant and extremophilic fungi are essential components. Some fungi are specialized in only one of these two environments and can thrive in conditions that are lethal to most other life-forms. Others are generalists, highly adaptable species that occur in both environments and tolerate a wide range of extremes. Both groups efficiently balance cellular osmotic pressure and ion concentration, stabilize cell membranes, remodel cell walls, and neutralize intracellular oxidative stress. Some species use unusual reproductive strategies. Further investigation of these adaptations with new methods and carefully designed experiments under ecologically relevant conditions will help predict the role of fungi in hypersaline and glacial environments affected by climate change, decipher their stress resistance mechanisms and exploit their biotechnological potential.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032521-020922
2023-09-15
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032521-020922.html?itemId=/content/journals/10.1146/annurev-micro-032521-020922&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Andreu C, Zarnowski R, del Olmo M. 2022. Recent developments in the biology and biotechnological applications of halotolerant yeasts. World J. Microbiol. Biotechnol. 38:227
    [Google Scholar]
  2. 2.
    Anesio AM, Laybourn-Parry J. 2012. Glaciers and ice sheets as a biome. Trends Ecol. Evol. 27:4219–25
    [Google Scholar]
  3. 3.
    Anesio AM, Lutz S, Chrismas NAM, Benning LG. 2017. The microbiome of glaciers and ice sheets. npj Biofilms Microbiomes 3:110
    [Google Scholar]
  4. 4.
    Azpiazu-Muniozguren M, Perez A, Rementeria A, Martinez-Malaxetxebarria I, Alonso R et al. 2021. Fungal diversity and composition of the continental solar saltern in Añana Salt Valley (Spain). J. Fungi. 7:121074
    [Google Scholar]
  5. 5.
    Baxter BK, Zalar P 2019. The extremophiles of Great Salt Lake: complex microbiology in a dynamic hypersaline ecosystem. Model Ecosystems in Extreme Environments J Seckbach, P Rampelotto 57–99. London: Elsevier
    [Google Scholar]
  6. 6.
    Bhuiyan M, Tucker D, Watson K. 2014. Gas chromatography-mass spectrometry analysis of fatty acid profiles of Antarctic and non-Antarctic yeasts. Antonie Van Leeuwenhoek 106:2381–89
    [Google Scholar]
  7. 7.
    Borovikova D, Muiznieks I, Rapoport A. 2015. New test-system based on the evaluation of yeast cells resistance to dehydration-rehydration stress. Open Biotechnol. J. 9:149–53
    [Google Scholar]
  8. 8.
    Brad T, Itcus C, Pascu M-D, Perşoiu A, Hillebrand-Voiculescu A et al. 2018. Fungi in perennial ice from Scărişoara Ice Cave (Romania). Sci. Rep. 8:110096
    [Google Scholar]
  9. 9.
    Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P. 2010. Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol. Ecol. 72:3354–69
    [Google Scholar]
  10. 10.
    Brown AJP, Larcombe DE, Pradhan A. 2020. Thoughts on the evolution of Core Environmental Responses in yeasts. Fungal Biol. 124:5475–81
    [Google Scholar]
  11. 11.
    Brown SP, Olson BJSC, Jumpponen A. 2015. Fungi and algae co-occur in snow: an issue of shared habitat or algal facilitation of heterotrophs?. Arctic Antarct. Alp. Res. 47:4729–49
    [Google Scholar]
  12. 12.
    Butinar L, Frisvad JC, Gunde-Cimerman N. 2011. Hypersaline waters—a potential source of foodborne toxigenic aspergilli and penicillia. FEMS Microbiol. Ecol. 77:1186–99
    [Google Scholar]
  13. 13.
    Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N 2005. Yeast diversity in hypersaline habitats. FEMS Microbiol. Lett. 244:2229–34
    [Google Scholar]
  14. 14.
    Butinar L, Sonjak S, Gunde-Cimerman N. 2009. Fungi in high Arctic glaciers. New Permafrost and Glacier Research MI Krugger, HP Stern 237–64. New York: Nova Sci.
    [Google Scholar]
  15. 15.
    Butinar L, Spencer-Martins I, Gunde-Cimerman N. 2007. Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. Antonie Van Leeuwenhoek 91:3277–89
    [Google Scholar]
  16. 16.
    Butinar L, Strmole T, Gunde-Cimerman N. 2011. Relative incidence of ascomycetous yeasts in Arctic coastal environments. Microb. Ecol. 61:4832–43
    [Google Scholar]
  17. 17.
    Butinar L, Zalar P, Frisvad JC, Gunde-Cimerman N. 2005. The genus Eurotium—members of indigenous fungal community in hypersaline waters of salterns. FEMS Microbiol. Ecol. 51:2155–66
    [Google Scholar]
  18. 18.
    Buzzini P, Turk M, Perini L, Turchetti B, Gunde-Cimerman N 2017. Yeasts in polar and subpolar habitats. Yeasts in Natural Ecosystems: Diversity P Buzzini, M-A Lachance, A Yurkov 331–65. Cham, Switz.: Springer
    [Google Scholar]
  19. 19.
    Calvillo-Medina RP, Gunde-Cimerman N, Escudero-Leyva E, Barba-Escoto L, Fernández-Tellez EI et al. 2020. Richness and metallo-tolerance of cultivable fungi recovered from three high altitude glaciers from Citlaltépetl and Iztaccíhuatl volcanoes (Mexico). Extremophiles 24:4625–36
    [Google Scholar]
  20. 20.
    Cantrell SA, Tkavc R, Gunde-Cimerman N, Zalar P, Acevedo M, Báez-Félix C. 2013. Fungal communities of young and mature hypersaline microbial mats. Mycologia 105:4827–36
    [Google Scholar]
  21. 21.
    Cao B, Haelewaters D, Schoutteten N, Begerow D, Boekhout T et al. 2021. Delimiting species in Basidiomycota: a review. Fungal Divers. 109:1181–237
    [Google Scholar]
  22. 22.
    Capusoni C, Arioli S, Donzella S, Guidi B, Serra I, Compagno C. 2019. Hyper-osmotic stress elicits membrane depolarization and decreased permeability in halotolerant marine Debaryomyces hansenii strains and in Saccharomyces cerevisiae. Front. Microbiol. 10:64
    [Google Scholar]
  23. 23.
    Chung D, Kim H, Choi HS. 2019. Fungi in salterns. J. Microbiol. 57:9717–24
    [Google Scholar]
  24. 24.
    de Garcia V, Brizzio S, Libkind D, Buzzini P, Van Broock M. 2007. Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol. Ecol. 59:2331–41
    [Google Scholar]
  25. 25.
    de Garcia V, Zalar P, Brizzio S, Gunde-Cimerman N, van Broock M. 2012. Cryptococcus species (Tremellales) from glacial biomes in the southern (Patagonia) and northern (Svalbard) hemispheres. FEMS Microbiol. Ecol. 82:2523–39
    [Google Scholar]
  26. 26.
    de Menezes GCA, Porto BA, Amorim SS, Zani CL, de Almeida Alves TM et al. 2020. Fungi in glacial ice of Antarctica: diversity, distribution and bioprospecting of bioactive compounds. Extremophiles 24:3367–76
    [Google Scholar]
  27. 27.
    D'Elia T, Veerapaneni R, Theraisnathan V, Rogers SO. 2009. Isolation of fungi from Lake Vostok accretion ice. Mycologia 101:6751–63
    [Google Scholar]
  28. 28.
    Duarte AWF, dos Santos JA, Vianna MV, Vieira JMF, Mallagutti VH et al. 2018. Cold-adapted enzymes produced by fungi from terrestrial and marine Antarctic environments. Crit. Rev. Biotechnol. 38:4600–19
    [Google Scholar]
  29. 29.
    Duo Saito RA, Connell L, Rodriguez R, Redman R, Libkind D, de Garcia V 2018. Metabarcoding analysis of the fungal biodiversity associated with Castaño Overa Glacier—Mount Tronador, Patagonia, Argentina. Fungal Ecol. 36:8–16
    [Google Scholar]
  30. 30.
    Ene IV, Walker LA, Schiavone M, Lee KK, Martin-Yken H et al. 2015. Cell wall remodeling enzymes modulate fungal cell wall elasticity and osmotic stress resistance. mBio 6:4e00986
    [Google Scholar]
  31. 31.
    Erdmann EA, Nitsche S, Gorbushina AA, Schumacher J. 2022. Genetic engineering of the rock inhabitant Knufia petricola provides insight into the biology of extremotolerant black fungi. Front. Fungal Biol. 3:862429
    [Google Scholar]
  32. 32.
    Feng L, Jia H, Qin Y, Song Y, Tao S, Liu Y. 2018. Rapid identification of major QTLs associated with near-freezing temperature tolerance in Saccharomyces cerevisiae. Front. Microbiol. 9:2110
    [Google Scholar]
  33. 33.
    Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R et al. 2005. A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol. Biol. Cell 16:42068–76
    [Google Scholar]
  34. 34.
    Gabaldón T. 2020. Hybridization and the origin of new yeast lineages. FEMS Yeast Res. 20:5foaa040
    [Google Scholar]
  35. 35.
    Gaidamakova EK, Sharma A, Matrosova VY, Grichenko O, Volpe RP et al. 2022. Small-molecule Mn antioxidants in Caenorhabditis elegans and Deinococcus radiodurans supplant MnSOD enzymes during aging and irradiation. mBio 13:1e0339421
    [Google Scholar]
  36. 36.
    Gašparič MBB, Lenassi M, Gostinčar C, Rotter A, Plemenitaš A et al. 2013. Insertion of a specific fungal 3′-phosphoadenosine-5′-phosphatase motif into a plant homologue improves halotolerance and drought tolerance of plants. PLOS ONE 8:12e81872
    [Google Scholar]
  37. 37.
    Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L et al. 2005. Biodiversity of cryopegs in permafrost. FEMS Microbiol. Ecol. 53:1117–28
    [Google Scholar]
  38. 38.
    Gocheva YG, Tosi S, Krumova ET, Slokoska LS, Miteva JG et al. 2009. Temperature downshift induces antioxidant response in fungi isolated from Antarctica. Extremophiles 13:2273–81
    [Google Scholar]
  39. 39.
    González-Abradelo D, Pérez-Llano Y, Peidro-Guzmán H, Sánchez-Carbente MDR, Folch-Mallol JL et al. 2019. First demonstration that ascomycetous halophilic fungi (Aspergillus sydowii and Aspergillus destruens) are useful in xenobiotic mycoremediation under high salinity conditions. Bioresour. Technol. 279:287–96
    [Google Scholar]
  40. 40.
    Gonzalez NA, Vázquez A, Ortiz Zuazaga HG, Sen A, Olvera HL et al. 2006. Genome-wide expression profiling of the osmoadaptation response of Debaryomyces hansenii. Yeast 26:2111–24
    [Google Scholar]
  41. 41.
    Gostinčar C, Grube M, Gunde-Cimerman N. 2011. Evolution of fungal pathogens in domestic environments?. Fungal Biol. 115:101008–18
    [Google Scholar]
  42. 42.
    Gostinčar C, Gunde-Cimerman N. 2018. Overview of oxidative stress response genes in selected halophilic fungi. Genes 9:3143
    [Google Scholar]
  43. 43.
    Gostinčar C, Gunde-Cimerman N, Turk M. 2012. Genetic resources of extremotolerant fungi: a method for identification of genes conferring stress tolerance. Bioresour. Technol. 111:360–67
    [Google Scholar]
  44. 44.
    Gostinčar C, Ohm RA, Kogej T, Sonjak S, Turk M et al. 2014. Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species. BMC Genom. 15:1549
    [Google Scholar]
  45. 45.
    Gostinčar C, Stajich JE, Kejžar A, Sinha S, Nislow C et al. 2021. Seven years at high salinity—experimental evolution of the extremely halotolerant black yeast Hortaea werneckii. J. Fungi. 7:9723
    [Google Scholar]
  46. 46.
    Gostinčar C, Sun X, Černoša A, Fang C, Gunde-Cimerman N, Song Z. 2022. Clonality, inbreeding, and hybridization in two extremotolerant black yeasts. GigaScience 11:giac095
    [Google Scholar]
  47. 47.
    Gostinčar C, Sun X, Zajc J, Fang C, Hou Y et al. 2019. Population genomics of an obligately halophilic basidiomycete Wallemia ichthyophaga. Front. Microbiol. 10:2019
    [Google Scholar]
  48. 48.
    Gostinčar C, Turk M, Trbuha T, Vaupotič T, Plemenitaš A, Gunde-Cimerman N. 2008. Expression of fatty-acid-modifying enzymes in the halotolerant black yeast Aureobasidium pullulans (de Bary) G. Arnaud under salt stress. Stud. Mycol. 61:6151–59
    [Google Scholar]
  49. 49.
    Gostinčar C, Turk M, Zajc J, Gunde-Cimerman N. 2019. Fifty Aureobasidium pullulans genomes reveal a recombining polyextremotolerant generalist. Environ. Microbiol. 21:103638–52
    [Google Scholar]
  50. 50.
    Gostinčar C, Zajc J, Lenassi M, Plemenitaš A, de Hoog S et al. 2018. Fungi between extremotolerance and opportunistic pathogenicity on humans. Fungal Divers. 93:1195–213
    [Google Scholar]
  51. 51.
    Gostinčar C, Zalar P, Gunde-Cimerman N. 2022. No need for speed: slow development of fungi in extreme environments. Fungal Biol. Rev. 39:1–14
    [Google Scholar]
  52. 52.
    Govrin R, Obstbaum T, Sivan U. 2019. Common source of cryoprotection and osmoprotection by osmolytes. J. Am. Chem. Soc. 141:3413311–14
    [Google Scholar]
  53. 53.
    Gunde-Cimerman N, Plemenitaš A. 2006. Ecology and molecular adaptations of the halophilic black yeast Hortaea werneckii. Rev. Environ. Sci. Biotechnol. 5:2323–31
    [Google Scholar]
  54. 54.
    Gunde-Cimerman N, Plemenitaš A, Oren A 2018. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol. Rev. 42:3353–75
    [Google Scholar]
  55. 55.
    Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B et al. 2003. Extremophilic fungi in Arctic ice: a relationship between adaptation to low temperature and water activity. Phys. Chem. Earth. 28:28–321273–78
    [Google Scholar]
  56. 56.
    Gunde-Cimerman N, Zalar P, Hoog S, Plemenitaš A. 2000. Hypersaline waters in salterns—natural ecological niches for halophilic black yeasts. FEMS Microbiol. Ecol. 32:3235–40
    [Google Scholar]
  57. 57.
    Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F. 2016. Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev. Environ. Sci. Bio/Technol. 15:2147–72
    [Google Scholar]
  58. 58.
    Hohmann S, Krantz M, Nordlander B. 2007. Yeast osmoregulation. Osmosensing and Osmosignaling H Sies, D Haeussinger 29–45. Methods Enzymol. 428 San Diego, CA: Elsevier
    [Google Scholar]
  59. 59.
    Jacques N, Zenouche A, Gunde-Cimerman N, Casaregola S. 2015. Increased diversity in the genus Debaryomyces from Arctic glacier samples. Antonie Van Leeuwenhoek 107:2487–501
    [Google Scholar]
  60. 60.
    Jančič S, Frisvad JC, Kocev D, Gostinčar C, Džeroski S, Gunde-Cimerman N. 2016. Production of secondary metabolites in extreme environments: Food- and airborne Wallemia spp. produce toxic metabolites at hypersaline conditions. PLOS ONE 11:12e0169116
    [Google Scholar]
  61. 61.
    Jančič S, Zalar P, Kocev D, Schroers H-J, Džeroski S, Gunde-Cimerman N. 2016. Halophily reloaded: new insights into the extremophilic life-style of Wallemia with the description of Wallemia hederae sp. nov. Fungal Divers. 76:197–118
    [Google Scholar]
  62. 62.
    Juvvadi PR, Lamoth F, Steinbach WJ. 2014. Calcineurin as a multifunctional regulator: unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis. Fungal Biol. Rev. 28:2–356–69
    [Google Scholar]
  63. 63.
    Kejžar A, Cibic M, Grøtli M, Plemenitaš A, Lenassi M. 2015. The unique characteristics of HOG pathway MAPKs in the extremely halotolerant Hortaea werneckii. FEMS Microbiol. Lett. 362:8fnv046
    [Google Scholar]
  64. 64.
    Khan NM-MU, Arai T, Tsuda S, Kondo H. 2021. Characterization of microbial antifreeze protein with intermediate activity suggests that a bound-water network is essential for hyperactivity. Sci. Rep. 11:15971
    [Google Scholar]
  65. 65.
    Kis-Papo T, Weig AR, Riley R, Persoh D, Salamov A et al. 2014. Genomic adaptations of the halophilic Dead Sea filamentous fungus Eurotium rubrum. Nat. Commun. 5:3745
    [Google Scholar]
  66. 66.
    Knowlton C, Veerapaneni R, D'Elia T, Rogers S 2013. Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology 2:1206–32
    [Google Scholar]
  67. 67.
    Kogej T, Gostinčar C, Volkmann M, Gorbushina AAA, Gunde-Cimerman N. 2006. Mycosporines in extremophilic fungi—novel complementary osmolytes?. Environ. Chem. 3:2105–10
    [Google Scholar]
  68. 68.
    Kogej T, Ramos J, Plemenitaš A, Gunde-Cimerman N. 2005. The halophilic fungus Hortaea werneckii and the halotolerant fungus Aureobasidium pullulans maintain low intracellular cation concentrations in hypersaline environments. Appl. Environ. Microbiol. 71:116600–5
    [Google Scholar]
  69. 69.
    Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-Cimerman N. 2007. Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology 153:Part 124261–73
    [Google Scholar]
  70. 70.
    Konte T, Terpitz U, Plemenitaš A. 2016. Reconstruction of the High-Osmolarity Glycerol (HOG) signaling pathway from the halophilic fungus Wallemia ichthyophaga in Saccharomyces cerevisiae. Front. Microbiol. 7:901
    [Google Scholar]
  71. 71.
    Kralj Kunčič M, Kogej T, Drobne D, Gunde-Cimerman N 2010. Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl. Environ. Microbiol. 76:1329–37
    [Google Scholar]
  72. 72.
    Lahav R, Fareleira P, Nejidat A, Abeliovich A. 2002. The identification and characterization of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microb. Ecol. 43:3388–96
    [Google Scholar]
  73. 73.
    Lee DW, Hong CP, Thak EJ, Park S, Lee CH et al. 2021. Integrated genomic and transcriptomic analysis reveals unique mechanisms for high osmotolerance and halotolerance in Hyphopichia yeast. Environ. Microbiol. 23:73499–522
    [Google Scholar]
  74. 74.
    Lenassi M, Zajc J, Gostinčar C, Gorjan A, Gunde-Cimerman N, Plemenitaš A. 2011. Adaptation of the glycerol-3-phosphate dehydrogenase Gpd1 to high salinities in the extremely halotolerant Hortaea werneckii and halophilic Wallemia ichthyophaga. Fungal Biol. 115:10959–70
    [Google Scholar]
  75. 75.
    Luo Y, Wei X, Yang S, Gao Y-H, Luo Z-H. 2020. Fungal diversity in deep-sea sediments from the Magellan seamounts as revealed by a metabarcoding approach targeting the ITS2 regions. Mycology 11:3214–29
    [Google Scholar]
  76. 76.
    Lutz S, Anesio AM, Edwards A, Benning LG. 2017. Linking microbial diversity and functionality of arctic glacial surface habitats. Environ. Microbiol. 19:2551–65
    [Google Scholar]
  77. 77.
    Maggi O, Tosi S, Angelova M, Lagostina E, Fabbri AA et al. 2013. Adaptation of fungi, including yeasts, to cold environments. Plant Biosyst. 147:1247–58
    [Google Scholar]
  78. 78.
    Martinelli L, Zalar P, Gunde-Cimerman N, Azua-Bustos A, Sterflinger K, Piñar G. 2017. Aspergillus atacamensis and A. salisburgensis: two new halophilic species from hypersaline/arid habitats with a phialosimplex-like morphology. Extremophiles 21:4755–73
    [Google Scholar]
  79. 79.
    Martínez-Ávila L, Peidro-Guzmán H, Pérez-Llano Y, Moreno-Perlín T, Sánchez-Reyes A et al. 2021. Tracking gene expression, metabolic profiles, and biochemical analysis in the halotolerant basidiomycetous yeast Rhodotorula mucilaginosa EXF-1630 during benzo[a]pyrene and phenanthrene biodegradation under hypersaline conditions. Environ. Pollut. 271:116358
    [Google Scholar]
  80. 80.
    Miteva V, Rinehold K, Sowers T, Sebastian A, Brenchley J. 2015. Abundance, viability and diversity of the indigenous microbial populations at different depths of the NEEM Greenland ice core. Polar Res. 34: https://doi.org/10.3402/polar.v34.25057
    [Google Scholar]
  81. 81.
    Muggia L, Zalar P, Azua-Bustos A, González-Silva C, Grube M, Gunde-Cimerman N. 2020. The beauty and the yeast: Can the microalgae Dunaliella form a borderline lichen with Hortaea werneckii?. Symbiosis 82:1–2123–31
    [Google Scholar]
  82. 82.
    Naranjo-Ortiz MA, Gabaldón T. 2019. Fungal evolution: major ecological adaptations and evolutionary transitions. Biol. Rev. 94:41443–76
    [Google Scholar]
  83. 83.
    Nazareth S, Gonsalves V. 2014. Aspergillus penicillioides—a true halophile existing in hypersaline and polyhaline econiches. Ann. Microbiol. 64:1397–402
    [Google Scholar]
  84. 84.
    Oren A. 1999. Bioenergetic aspects of halophilism. Microbiol. Mol. Biol. Rev. 63:2334–48
    [Google Scholar]
  85. 85.
    Orfali RS, Aly AH, Ebrahim W, Rudiyansyah Proksch P. 2015. Isochroman and isocoumarin derivatives from hypersaline lake sediment-derived fungus Penicillium sp. Phytochem. Lett. 13:234–38
    [Google Scholar]
  86. 86.
    Palumbo RJ, McKean N, Leatherman E, Namitz KEW, Connell L et al. 2022. Coevolution of the Ess1-CTD axis in polar fungi suggests a role for phase separation in cold tolerance. Sci. Adv. 8:36eabq3235
    [Google Scholar]
  87. 87.
    Panadero J, Hernaández-López MJ, Prieto JA, Randez-Gil F. 2007. Overexpression of the calcineurin target CRZ1 provides freeze tolerance and enhances the fermentative capacity of baker's yeast. Appl. Environ. Microbiol. 73:154824–31
    [Google Scholar]
  88. 88.
    Panadero J, Pallotti C, Rodríguez-Vargas S, Randez-Gil F, Prieto JA. 2006. A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J. Biol. Chem. 281:84638–45
    [Google Scholar]
  89. 89.
    Papouskova K, Sychrova H. 2007. The co-action of osmotic and high temperature stresses results in a growth improvement of Debaryomyces hansenii cells. Int. J. Food Microbiol. 118:11–7
    [Google Scholar]
  90. 90.
    Pérez-Llano Y, Rodríguez-Pupo EC, Druzhinina IS, Chenthamara K, Cai F et al. 2020. Stress reshapes the physiological response of halophile fungi to salinity. Cells 9:3525
    [Google Scholar]
  91. 91.
    Perini L, Andrejašič K, Gostinčar C, Gunde-Cimerman N, Zalar P. 2021. Greenland and Svalbard glaciers host unknown basidiomycetes: the yeast Camptobasidium arcticum sp. nov. and the dimorphic Psychromyces glacialis gen. and sp. nov. Int. J. Syst. Evol. Microbiol. 71:2004655
    [Google Scholar]
  92. 92.
    Perini L, Gostinčar C, Anesio AMAM, Williamson C, Tranter M, Gunde-Cimerman N. 2019. Darkening of the Greenland Ice Sheet: fungal abundance and diversity are associated with algal bloom. Front. Microbiol. 10:557
    [Google Scholar]
  93. 93.
    Perini L, Gostinčar C, Gunde-Cimerman N. 2019. Fungal and bacterial diversity of Svalbard subglacial ice. Sci. Rep. 9:120230
    [Google Scholar]
  94. 94.
    Perini L, Gostinčar C, Likar M, Frisvad JC, Kostanjšek R et al. 2023. Interactions of fungi and algae from the Greenland Ice Sheet. Microb. Ecol. 86:282–96
    [Google Scholar]
  95. 95.
    Perini L, Mogrovejo DC, Tomazin R, Gostinčar C, Brill FHH, Gunde-Cimerman N. 2019. Phenotypes associated with pathogenicity: their expression in Arctic fungal isolates. Microorganisms 7:12600
    [Google Scholar]
  96. 96.
    Petelenz-Kurdziel E, Eriksson E, Smedh M, Beck C, Hohmann S, Goksör M. 2011. Quantification of cell volume changes upon hyperosmotic stress in Saccharomyces cerevisiae. Integr. Biol. 3:111120–26
    [Google Scholar]
  97. 97.
    Petrovič U. 2006. Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Res. 6:5816–22
    [Google Scholar]
  98. 98.
    Plemenitaš A. 2021. Sensing and responding to hypersaline conditions and the HOG signal transduction pathway in fungi isolated from hypersaline environments: Hortaea werneckii and Wallemia ichthyophaga. J. Fungi. 7:11988
    [Google Scholar]
  99. 99.
    Prista C, Loureiro-Dias MC, Montiel V, Garcia R, Ramos J et al. 2005. Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res. 5:8693–701
    [Google Scholar]
  100. 100.
    Prista C, Michán C, Miranda IM, Ramos J. 2016. The halotolerant Debaryomyces hansenii, the Cinderella of non-conventional yeasts. Yeast 33:10523–33
    [Google Scholar]
  101. 101.
    Pusz W, Urbaniak J. 2021. Airborne fungi in Longyearbyen area (Svalbard, Norway)—case study. Environ. Monit. Assess. 193:5290
    [Google Scholar]
  102. 102.
    Raghupathi PK, Zupančič J, Brejnrod AD, Jacquiod S, Houf K et al. 2018. Microbial diversity and putative opportunistic pathogens in dishwasher biofilm communities. Appl. Environ. Microbiol. 84:5e02755–17
    [Google Scholar]
  103. 103.
    Rossi M, Buzzini P, Cordisco L, Amaretti A, Sala M et al. 2009. Growth, lipid accumulation, and fatty acid composition in obligate psychrophilic, facultative psychrophilic, and mesophilic yeasts. FEMS Microbiol. Ecol. 69:3363–72
    [Google Scholar]
  104. 104.
    Russell NJ 2008. Membrane components and cold sensing. Psychrophiles: From Biodiversity to Biotechnology R Margesin, F Schinner, J-C Marx, C Gerday 177–90. Berlin: Springer
    [Google Scholar]
  105. 105.
    Šantl-Temkiv T, Lange R, Beddows D, Rauter U, Pilgaard S et al. 2019. Biogenic sources of ice nucleating particles at the High Arctic site Villum Research Station. Environ. Sci. Technol. 53:1810580–90
    [Google Scholar]
  106. 106.
    Sharma A, Gaidamakova EK, Grichenko O, Matrosova VY, Hoeke V et al. 2017. Across the tree of life, radiation resistance is governed by antioxidant Mn2+, gauged by paramagnetic resonance. PNAS 114:44E9253–60
    [Google Scholar]
  107. 107.
    Sklenář F, Jurjević Ž, Zalar P, Frisvad JC, Visagie CM et al. 2017. Phylogeny of xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section Restricti. Stud. Mycol. 88:161–236
    [Google Scholar]
  108. 108.
    Soler-Hurtado MM, Sandoval-Sierra JV, Machordom A, Diéguez-Uribeondo J. 2016. Aspergillus sydowii and other potential fungal pathogens in gorgonian octocorals of the Ecuadorian Pacific. PLOS ONE 11:11e0165992
    [Google Scholar]
  109. 109.
    Sonjak S, Frisvad JC, Gunde-Cimerman N. 2005. Comparison of secondary metabolite production by Penicillium crustosum strains, isolated from Arctic and other various ecological niches. FEMS Microbiol. Ecol. 53:151–60
    [Google Scholar]
  110. 110.
    Sonjak S, Frisvad JC, Gunde-Cimerman N. 2006. Penicillium mycobiota in Arctic subglacial ice. Microb. Ecol. 52:2207–16
    [Google Scholar]
  111. 111.
    Sonjak S, Frisvad JC, Gunde-Cimerman N. 2007. Genetic variation among Penicillium crustosum isolates from Arctic and other ecological niches. Microb. Ecol. 54:2298–305
    [Google Scholar]
  112. 112.
    Sonjak S, Frisvad JC, Gunde-Cimerman N. 2009. Fingerprinting using extrolite profiles and physiological data shows sub-specific groupings of Penicillium crustosum strains. Mycol. Res. 113:8836–41
    [Google Scholar]
  113. 113.
    Starmer WT, Fell YW, Catranis CM, Aberdeen V, Ma LJ et al. 2005. Yeasts in the genus Rhodotorula recovered from the Greenland ice sheet. Life in Ancient Ice JD Castello, SO Rogers 181–95. Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  114. 114.
    Sterflinger K, Lopandic K, Pandey RV, Blasi B, Kriegner A. 2014. Nothing special in the specialist? Draft genome sequence of Cryomyces antarcticus, the most extremophilic fungus from Antarctica. PLOS ONE 9:10e109908
    [Google Scholar]
  115. 115.
    Su Y, Jiang X, Wu W, Wang M, Hamid MI et al. 2016. Genomic, transcriptomic, and proteomic analysis provide insights into the cold adaptation mechanism of the obligate psychrophilic fungus Mrakia psychrophila. G3 6:113603–13
    [Google Scholar]
  116. 116.
    Sun X, Gostinčar C, Fang C, Zajc J, Hou Y et al. 2019. Genomic evidence of recombination in the basidiomycete Wallemia mellicola. Genes 10:6427
    [Google Scholar]
  117. 117.
    Tafer H, Poyntner C, Lopandic K, Sterflinger K, Piñar G. 2019. Back to the salt mines: genome and transcriptome comparisons of the halophilic fungus Aspergillus salisburgensis and its halotolerant relative Aspergillus sclerotialis. Genes 10:5381
    [Google Scholar]
  118. 118.
    Tai SL, Daran-Lapujade P, Walsh MC, Pronk JT, Daran J-M. 2007. Acclimation of Saccharomyces cerevisiae to low temperature: a chemostat-based transcriptome analysis. Mol. Biol. Cell 18:125100–12
    [Google Scholar]
  119. 119.
    Tamás MJ, Luyten K, Sutherland FC, Hernandez A, Albertyn J et al. 1999. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol. 31:41087–104
    [Google Scholar]
  120. 120.
    Tanaka T, Nishio K, Usuki Y, Fujita K-I. 2006. Involvement of oxidative stress induction in Na+ toxicity and its relation to the inhibition of a Ca2+-dependent but calcineurin-independent mechanism in Saccharomyces cerevisiae. J. Biosci. Bioeng. 101:177–79
    [Google Scholar]
  121. 121.
    Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T et al. 2010. Cold-adapted yeasts from Antarctica and the Italian Alps—description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:147–59
    [Google Scholar]
  122. 122.
    Todd RT, Forche A, Selmecki A. 2017. Ploidy variation in fungi: polyploidy, aneuploidy, and genome evolution. Microbiol. Spectr. 5:45.4.09
    [Google Scholar]
  123. 123.
    Touchette D, Altshuler I, Gostinčar C, Zalar P, Raymond-Bouchard I et al. 2022. Novel Antarctic yeast adapts to cold by switching energy metabolism and increasing small RNA synthesis. ISME J 16:1221–32
    [Google Scholar]
  124. 124.
    Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G et al. 2008. Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol. Ecol. 63:173–83
    [Google Scholar]
  125. 125.
    Turchetti B, Goretti M, Branda E, Diolaiuti G, D'Agata C et al. 2013. Influence of abiotic variables on culturable yeast diversity in two distinct Alpine glaciers. FEMS Microbiol. Ecol. 86:2327–40
    [Google Scholar]
  126. 126.
    Turchetti B, Thomas Hall SR, Connell LB, Branda E, Buzzini P et al. 2011. Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:5573–86
    [Google Scholar]
  127. 127.
    Turk M, Gostinčar C. 2018. Glycerol metabolism genes in Aureobasidium pullulans and Aureobasidium subglaciale. Fungal Biol. 122:163–73
    [Google Scholar]
  128. 128.
    Turk M, Méjanelle L, Šentjurc M, Grimalt JO, Gunde-Cimerman N, Plemenitaš A. 2004. Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 8:153–61
    [Google Scholar]
  129. 129.
    Turk M, Plemenitaš A. 2002. The HOG pathway in the halophilic black yeast Hortaea werneckii: isolation of the HOG1 homolog gene and activation of HwHog1p. FEMS Microbiol. Lett. 216:2193–99
    [Google Scholar]
  130. 130.
    Vaupotič T, Gunde-Cimerman N, Plemenitaš A. 2007. Novel 3′-phosphoadenosine-5′-phosphatases from extremely halotolerant Hortaea werneckii reveal insight into molecular determinants of salt tolerance of black yeasts. Fungal Genet. Biol. 44:111109–22
    [Google Scholar]
  131. 131.
    Vaupotič T, Plemenitaš A. 2007. Differential gene expression and HogI interaction with osmoresponsive genes in the extremely halotolerant black yeast Hortaea werneckii. BMC Genom. 8:1280–95
    [Google Scholar]
  132. 132.
    Vishniac HS. 2002. Cryptococcus tephrensis, sp.nov., and Cryptococcus heimaeyensis, sp.nov.: new anamorphic basidiomycetous yeast species from Iceland. Can. J. Microbiol. 48:5463–67
    [Google Scholar]
  133. 133.
    Wasser SP, Grishkan I, Buchalo AS, Kis-Papo T, Volz PA et al. 2003. Species diversity of the Dead Sea. Fungal Life in the Dead Sea E Nevo, A Oren, SP Wasser 203–70. Ruggell, Liechtenst.: A.R.G. Gantner Verlag
    [Google Scholar]
  134. 134.
    Wei Y-L, Long Z-J, Ren M-X. 2022. Microbial community and functional prediction during the processing of salt production in a 1000-year-old marine solar saltern of South China. Sci. Total Environ. 819:152014
    [Google Scholar]
  135. 135.
    Zajc J, Černoša A, Sun X, Fang C, Gunde-Cimerman N et al. 2022. From glaciers to refrigerators: the population genomics and biocontrol potential of the black yeast Aureobasidium subglaciale. Microbiol. Spectr. 10:4e0145522
    [Google Scholar]
  136. 136.
    Zajc J, Džeroski S, Kocev D, Oren A, Sonjak S et al. 2014. Chaophilic or chaotolerant fungi: a new category of extremophiles?. Front. Microbiol. 5:708
    [Google Scholar]
  137. 137.
    Zajc J, Gunde-Cimerman N. 2018. The genus Wallemia—from contamination of food to health threat. Microorganisms 6:246
    [Google Scholar]
  138. 138.
    Zajc J, Kogej T, Ramos J, Galinski EA, Gunde-Cimerman N. 2014. The osmoadaptation strategy of the most halophilic fungus Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl. Environ. Microbiol. 80:1247–56
    [Google Scholar]
  139. 139.
    Zajc J, Liu Y, Dai W, Yang Z, Hu J et al. 2013. Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: Haloadaptations present and absent. BMC Genom. 14:617
    [Google Scholar]
  140. 140.
    Zajc J, Zalar P, Gunde-Cimerman N. 2017. Yeasts in hypersaline habitats. Yeasts in Natural Ecosystems: Diversity293–329. Cham, Switz: Springer
    [Google Scholar]
  141. 141.
    Zalar P, de Hoog GS, Schroers H-J, 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. 58:1157–83
    [Google Scholar]
  142. 142.
    Zalar P, Frisvad JC, Gunde-Cimerman N, Varga J, Samson RA. 2008. Four new species of Emericella from the Mediterranean region of Europe. Mycologia 100:5779–95
    [Google Scholar]
  143. 143.
    Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M, Gunde-Cimerman N. 2008. Redefinition of Aureobasidium pullulans and its varieties. Stud. Mycol. 61:21–38
    [Google Scholar]
  144. 144.
    Zalar P, Kocuvan MA, Plemenitaš A, Gunde-Cimerman N. 2005. Halophilic black yeasts colonize wood immersed in hypersaline water. Bot. Mar. 48:4323–26
    [Google Scholar]
  145. 145.
    Zalar P, Novak M, De Hoog GS, Gunde-Cimerman N. 2011. Dishwashers—a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol. 115:10997–1007
    [Google Scholar]
  146. 146.
    Zalar P, Sonjak S, Gunde-Cimerman N 2011. Fungi in polar environments. Polar Microbiology: Life in a Deep Freeze RB Miller, LG Whyte 79–99. Washington, DC: ASM
    [Google Scholar]
  147. 147.
    Zalar P, Sybren de Hoog G, Schroers H-J, Frank JM, Gunde-Cimerman N. 2005. Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek 87:4311–28
    [Google Scholar]
  148. 148.
    Zhang T, Wang N-F, Yu L-Y. 2021. Geographic distance and habitat type influence fungal communities in the Arctic and Antarctic sites. Microb. Ecol. 82:1224–32
    [Google Scholar]
  149. 149.
    Zhang Z, Lu Y, Chi Z, Liu G-L, Jiang H et al. 2019. Genome editing of different strains of Aureobasidium melanogenum using an efficient Cre/loxp site-specific recombination system. Fungal Biol. 123:10723–31
    [Google Scholar]
  150. 150.
    Zupančič J, Raghupathi PK, Houf K, Burmølle M, Sørensen SJ, Gunde-Cimerman N. 2018. Synergistic interactions in microbial biofilms facilitate the establishment of opportunistic pathogenic fungi in household dishwashers. Front. Microbiol. 9:21
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032521-020922
Loading
/content/journals/10.1146/annurev-micro-032521-020922
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error