Chaophilic or chaotolerant fungi: A new category of extremophiles?

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Zajc, Janja ^a   Džeroski, Sašo ^b,c   Kocev, Dragi ^b   Oren, Aharon ^d   Sonjak, Silva ^a   Tkavc, Rok ^a,e   Gunde Cimerman, Nina ^a,c  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

^c Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP)   (Slovenia)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Calcium chloride; Chaotropes; Halophiles; Kosmotropes; Life limit; Magnesium chloride; Xerophiles

Indexed keywords

CALCIUM CHLORIDE; MAGNESIUM CHLORIDE;

ARTICLE; ASPERGILLUS AMSTELODAMI; CHAOPHILIC FUNGUS; CHAOTOLERANT FUNGUS; CLADOSPORIUM; DATA ANALYSIS; EUROTIUM CHEVALIERI; FUNGUS; FUNGUS GROWTH; HORTAEA WERNECKII; MACHINE LEARNING; MICROSCOPY; NONHUMAN; OPTICAL DENSITY; PENICILLIUM; SALINITY; SCREENING; TAXONOMIC RANK;

EUKARYOTA; EUROTIUM AMSTELODAMI; EUROTIUM CHEVALIERI; FUNGI; HORTAEA WERNECKII; PROKARYOTA; WALLEMIA ICHTHYOPHAGA;

EID: 84920667494     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00708     Document Type: Article

References (59)

1. Abdel-Hafez, S., Maubasher, A., and Abdel-Fattah, H. (1978). Cellulose-decomposing fungi of salt marshes in Egypt. Folia Microbiol. (Praha). 23, 37-44. doi: 10.1007/bf02876594
2. Ariño, J., Ramos, J., and Sychrova, H. (2010). Alkali metal cation transport and homeostasis in yeasts. Microbiol. Mol. Biol. Rev. 74, 95-120. doi: 10.1128/Mmbr.00042-09
3. Baas Becking, L. G. M. (1934). Geobiologie of Inleiding tot de Milieukunde. Den Haag: W.P. Van Stockum & Zoon N.V.
4. Butinar, L., Frisvad, J. C., and Gunde-Cimerman, N. (2011). Hypersaline waters - a potential source of foodborne toxigenic aspergilli and penicillia. FEMS Microbiol. Ecol. 77, 186-199. doi: 10.1111/j.1574-6941.2011.01108.x
5. Butinar, L., Santos, S., Spencer-Martins, I., Oren, A., and Gunde-Cimerman, N. (2005a). Yeast diversity in hypersaline habitats. FEMS Microbiol. Lett. 244, 229-234. doi: 10.1016/j.femsle.2005.01.043
6. Butinar, L., Sonjak, S., Zalar, P., Plemenitaš, A., and Gunde-Cimerman, N. (2005b). Melanized halophilic fungi are eukaryotic members of microbial communities in hypersaline waters of solar salterns. Botanica Marina 48, 73-79. doi: 10.1515/Bot.2005.007
7. Butinar, L., Zalar, P., Frisvad, J. C., and Gunde-Cimerman, N. (2005c). The genus Eurotium - members of indigenous fungal community in hypersaline waters of salterns. FEMS Microbiol. Ecol. 51, 155-166. doi: 10.1016/j.femsec.2004.08.002
8. Cantrell, S. A., Casillas-Martinez, L., and Molina, M. (2006). Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol. Res. 110, 962-970. doi: 10.1016/j.mycres.2006.06.005
9. Ferreira, C., Van Voorst, F., Martins, A., Neves, L., Oliveira, R., Kielland-Brandt, M. C., et al. (2005). A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 2068-2076. doi: 10.1091/mbc.E04-10-0884
10. Gorjan, A., and Plemenitaš, A. (2006). Identification and characterization of ENA ATPases HwENA1 and HwENA2 from the halophilic black yeast Hortaea werneckii. FEMS Microbiol. Lett. 265, 41-50. doi: 10.1111/j.1574-6968.2006.00473.x
11. Gostinčar, C., Grube, M., de Hoog, S., Zalar, P., and Gunde-Cimerman, N. (2010). Extremotolerance in fungi: evolution on the edge. FEMS Microbiol. Ecol. 71, 2-11. doi: 10.1111/j.1574-6941.2009.00794.x
12. Gostinčar, C., Lenassi, M., Gunde-Cimermna, N., and Plemenitaš, A. (2011). Fungal adaptation to extremely high salt concentrations. Adv. Appl. Microbiol. 77, 71-96. doi: 10.1016/B978-0-12-387044-5.00003-0
13. Gostinčar, C., Ohm, R., Kogej, T., Sonjak, S., Turk, M., Zajc, J., et al. (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
14. Gunde-Cimerman, N., Sonjak, S., Zalar, P., Frisvad, J. C., Diderichsen, B., and Plemenitas, A. (2003). Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys. Chem. Earth 28, 1273-1278. doi: 10.1016/j.pce.2003.08.056
15. Gunde-Cimerman, N., Zalar, P., de Hoog, S., and Plemenitaš, A. (2000). Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. FEMS Microbiol. Ecol. 32, 235-240. doi: 10.1111/j.1574-6941.2000.tb00716.x
16. Hallsworth, J. E., Yakimov, M. M., Golyshin, P. N., Gillion, J. L., D'auria, G., De Lima Alves, F., et al. (2007). Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ. Microbiol. 9, 801-813. doi: 10.1111/j.1462-2920.2006.01212.x
17. Hocking, A. D., Miscamble, B. F., and Pitt, J. I. (1994). Water relations of Alternaria alternata, Cladosporium cladosporioides, Cladosporium sphaerospermum, Curvularia lunata and Curvularia pallescens. Mycol. Res. 98, 91-94. doi: 10.1016/s0953-7562(09)80344-4
18. Hofmeister, F. (1888). Zur Lehre von der Wirkung der Salze. Zweite Mittheilung. Archiv. Exp. Pathol. Pharmakol. 247-260.
19. Hohmann, S. (2009). Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett. 583, 4025-4029. doi: 10.1016/j.febslet.2009.10.069
20. Jacobson, E. S., and Ikeda, R. (2005). Effect of melanization upon porosity of the cryptococcal cell wall. Med. Mycol. 43, 327-333. doi: 10.1080/13693780412331271081
21. Javor, B. J. (1989). "Hypersaline environments," in Microbiology and Biogeochemistry, ed U. Schiewer (Berlin: Springer-Verlag Berlin and Heidelberg GmbH & Co. K), 287-287.
22. Kocev, D., Vens, C., Struyf, J., and Dzeroski, S. (2013). Tree ensembles for predicting structured outputs. Pattern Recogn. 46, 817-833. doi: 10.1016/j.patcog.2012.09.023
23. Kogej, T., Gorbushina, A. A., and Gunde-Cimerman, N. (2006). Hypersaline conditions induce changes in cell-wall melanization and colony structure in a halophilic and a xerophilic black yeast species of the genus Trimmatostroma. Mycol. Res. 110, 713-724. doi: 10.1016/j.mycres.2006.01.014
24. Kogej, T., Ramos, J., Plemenitaš, A., and 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, 6600-6605. doi: 10.1128/AEM.71.11.6600-6605.2005
25. Kogej, T., Stein, M., Volkmann, M., Gorbushina, A. A., Galinski, E. A., and Gunde-Cimerman, N. (2007). Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology 153, 4261-4273. doi: 10.1099/mic.0.2007/010751-0
26. Kralj Kunčič, M., Kogej, T., Drobne, D., and Gunde-Cimerman, N. (2010). Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl. Environ. Microbiol. 76, 329-337. doi: 10.1128/AEM.02318-09
27. Kunz, W., Henle, J., and Ninham, B. W. (2004). "Zur Lehre von der Wirkung der Salze" (about the science of the effect of salts): Franz Hofmeister's historical papers. Curr. Opin. Colloid Interface Sci. 9, 19-37. doi: 10.1016/j.cocis.2004.05.005
28. Lenassi, M., Gostinèar, C., Jackman, S., Turk, M., Sadowski, I., Nislow, C., et al. (2013). Whole genome duplication and enrichment of metal cation transporters revealed by de novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii. PLoS ONE 8:e71328. doi: 10.1371/journal.pone.0071328
29. Leong, S.-L. L., Lantz, H., Pettersson, O. V., Frisvad, J. C., Thrane, U., Heipieper, H. J., et al. (2014). Genome and physiology of the ascomycete filamentous fungus Xeromyces bisporus, the most xerophilic organism isolated to date. Environ. Microbiol. doi: 10.1111/1462-2920.12596. [Epub ahead of print].
30. Levatić, J., Kocev, D., and Džeroski, S. (2014). "The use of the label hierarchy in hierarchical multi-label classification improves performance," in New Frontiers in Mining Complex Patterns, eds A. Appice, M. Ceci, C. Loglisci, G. Manco, E. Masciari and Z. W. Ras (Heidelberg: Springer International Publishing), 162-177. doi: 10.1007/978-3-319-08407-7_11
31. Luyten, K., Albertyn, J., Skibbe, W. F., Prior, B. A., Ramos, J., Thevelein, J. M., et al. (1995). Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14, 1360-1371.
32. McGenity, T. J., and Oren, A. (2012). "Life in saline environments," in Life at Extremes. Environments, Organisms and Strategies for Survival, ed E. M. Bell (Walling Ford, UK: CABI International), 402-437.
33. Mullakhanbhai, M. F., and Larsen, H. (1975). Halobacterium volcanii spec. nov., a Dead Sea halobacterium with a moderate salt requirement. Arch. Microbiol. 104, 207-214.
34. Oren, A. (1983). Halobacterium sodomense sp. nov., a Dead-Sea halobacterium with an extremely high magnesium requirement. Int. J. Syst. Bacteriol. 33, 381-386.
35. Oren, A. (2002). Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J. Ind. Microbiol. Biotechnol. 28, 56-63. doi: 10.1038/sj/jim/7000176
36. Oren, A. (2011). "The halophilic world of Lourens Baas Becking," in Halophiles and Hypersaline Environments: Current Research and Future Trends, eds A. Ventosa, A. Oren and Y. Ma (Heidelberg;Dordrecht;London;New York, NY: Springer-Verlag), 215-232.
37. Oren, A. (2013). "Life in magnesium- and calcium-rich hypersaline environments: salt stress by chaotropic ions," in Polyextremophiles, eds J. Seckbach, A. Oren and H. Stan-Lotter (Dordrecht: Springer Netherlands), 215-232.
38. Oren, A., and Gunde-Cimerman, N. (2012). "Fungal life in the Dead Sea," in Biology of Marine Fungi, ed C. Raghukumar (Berlin Heidelberg: Springer-Verlag), 115-132.
39. Oren, A., Gurevich, P., Gemmell, R. T., and Teske, A. (1995). Halobaculum gomorrense gen. nov., sp. nov, a novel extremely halophilic archaeon from the Dead-Sea. Int. J. Syst. Bacteriol. 45, 747-754.
40. Palkova, Z. (2004). Multicellular microorganisms: laboratory versus nature. EMBO Rep. 5, 470-476. doi: 10.1038/sj.embor.7400145
41. Palkova, Z., and Vachova, L. (2006). Life within a community: benefit to yeast long-term survival. FEMS Microbiol. Rev. 30, 806-824. doi: 10.1111/j.1574-6976.2006.00034.x
42. Pitt, J. I., and Hocking, A. D. (1977). Influence of solute and hydrogen-ion concentration on water relations of some xerophilic fungi. J. Gen. Microbiol. 101, 35-40.
43. Pitt, J. I., and Hocking, A. D. (2009). Fungi and Food Spoilage. Dordrecht: Springer.
44. Samson, R. A., Hoekstra, E. S., Frisvad, J. C., and Filtenborg, O. (2002). Introduction to Food- and Airborne Fungi. Baarn: Centraalbureau voor Schimmelcultures.
45. 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. Stud. Mycol. 51, 1-32.
46. Sonjak, S., Frisvad, J. C., and Gunde-Cimerman, N. (2006). Penicillium mycobiota in Arctic subglacial ice. Microb. Ecol. 52, 207-216. doi: 10.1007/s00248-006-9086-0
47. Sonjak, S., Gürsu, B., and Gunde-Cimerman, N. (2010). "MgCl2 tolerant fungi from the bitterns," in 8th International Congress on Extremophiles AZORES 2010 (Ponta Delgada), 109.
48. Stevenson, A., Burkhardt, J., Cockell, C. S., Cray, J. A., Dijksterhuis, J., Fox-Powell, M., et al. (2014). Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ. Microbiol. doi: 10.1111/1462-2920.12598. [Epub ahead of print].
49. Tresner, H. D., and Hayes, J. A. (1971). Sodium chloride tolerance of terrestrial fungi. Appl. Microbiol. 22, 210-213.
50. van Der Wielen, P. W., Bolhuis, H., Borin, S., Daffonchio, D., Corselli, C., Giuliano, L., et al. (2005). The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307, 121-123. doi: 10.1126/science.1103569
51. Vens, C., Struyf, J., Schietgat, L., Dzeroski, S., and Blockeel, H. (2008). Decision trees for hierarchical multi-label classification. Mach. Learn. 73, 185-214. doi: 10.1007/s10994-008-5077-3
52. Williams, J. P., and Hallsworth, J. E. (2009). Limits of life in hostile environments: no barriers to biosphere function? Environ. Microbiol. 11, 3292-3308. doi: 10.1111/j.1462-2920.2009.02079.x
53. Wollenzien, U., de Hoog, G. S., Krumbein, W. E., and Urzi, C. (1995). On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Sci. Total Environ. 167, 287-294. doi: 10.1016/0048-9697(95)04589-S
54. Zajc, J., Kogej, T., Ramos, J., Galinski, E. A., and 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, 247-256. doi: 10.1128/AEM.02702-13
55. Zajc, J., Liu, Y., Dai, W., Yang, Z., Hu, J., Gostinèar, C., et al. (2013). Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 14:617. doi: 10.1186/1471-2164-14-617
56. Zajc, J., Zalar, P., Plemenitaš, A., and Gunde-Cimerman, N. (2012). "The Mycobiota of the Salterns," in Biology of Marine Fungi, ed C. Raghukumar (Berlin Heidelberg: Springer-Verlag), 133-158.
57. Zalar, P., de Hoog, G. S., Schroers, H. J., Crous, P. W., Groenewald, J. Z., and 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, 157-183. doi: 10.3114/sim.2007.58.06
58. Zalar, P., de Hoog, G. S., Schroers, H. J., Frank, J. M., and Gunde-Cimerman, N. (2005). Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie van Leeuwenhoek 87, 311-328. doi: 10.1007/s10482-004-6783-x
59. Zhang, Y., and Cremer, P. S. (2006). Interactions between macromolecules and ions: the Hofmeister series. Curr. Opin. Chem. Biol. 10, 658-663. doi: 10.1016/j.cbpa.2006.09.020