Adaptation of extremely halotolerant black yeast Hortaea werneckii to increased osmolarity: a molecular perspective at a glance

Studies in Mycology

Volumn 61, Issue , 2008, Pages 67-75

  Plemenitaš, A ^a   Vaupotič, T ^a   Lenassi, M ^a   Kogej, T ^a   Gunde Cimerman, N ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Compatible solutes; Differential gene expression; Hal2; Halophile; HOG signaling pathway; Hortaea werneckii; Hypersaline water; Ions; Melanin

Indexed keywords

CHAETOTHYRIALES; EUKARYOTA; HORTAEA WERNECKII; PROKARYOTA;

EID: 59249106233     PISSN: 01660616     EISSN: None     Source Type: Journal    
DOI: 10.3114/sim.2008.61.06     Document Type: Article

References (75)

1. Alepuz PM, de Nadal E, Zapater M, Ammerer G, Posas F (2003). Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO Journal 22:2433-2442.
2. Alepuz PM, Jovanovic A, Reiser V, Ammerer G (2001). Stress-induced map kinase Hog1 is part of transcription activation complexes. Molecular Cell 7:767-777.
3. Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J, Loureiro-Dias MC (2000). Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions.International Journal of Food Microbiology 56:191-197.
4. Andersson A, Jordan D, Schneider G, Lindqvist Y (1996). Crystal structure of the ternary complex of 1,3,8-trihydroxynaphthalene reductase from Magnaporthe grisea with NADPH and an active-site inhibitor. Structure 4:1161-1170.
5. Andre L, Nillsson A, Adler L (1988). The role of glycerol in osmotolerance of the yeast Debaromyces hansenii.Journal of Genetics and Microbiology 134:669-677.
6. Bandaranayake WM (1998). Mycosporines: are they nature's sunscreens? Natural Product Reports 15:159-172.
7. Blomberg A (2000). Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiology Letters 182:1-8.
8. Blomberg A, Adler L (1992). Physiology of osmotolerance in fungi. Advances in Microbial Physiology 33:145-212.
9. Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005). Yeast diversity in hypersaline habitats. FEMS Microbiology Letters 244:229-234.
10. Cantrell SA, Casillas-Martínez L, Molina M (2006). Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycological Research 110:962-970.
11. Catlett NL, Yoder OC, Turgeon BG (2003). Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell 2:1151-1161.
12. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001). Remodeling of yeast genome expression in response to environmental changes. Molecular Biology of the Cell 12:323-337.
13. Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K (2005). Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Molecular Microbiology 56:1246-1261.
14. Gacto M, Soto T, Vicente-Soler J, Villa TG, Cansado J (2003). Learning from yeasts: intracellular sensing of stress conditions. International Microbiology 6:211-219.
15. Göttlich E, Hoog GS de, Yoshida S, Takeo K, Nishimura K, Miyaji M (1995). Cell-surface hydrophobicity and lipolysis as essential factors in human tinea nigra. Mycoses 38:489-494.
16. Gunde-Cimerman N, Zalar P, Hoog GS de, Plemenitaš A (2000). Hypersaline waters in salterns: natural ecological niches for halophilic black yeasts. FEMS Microbiology Ecology 32:235-340.
17. Han KH, Prade RA (2002). Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Molecular Microbiology 43:1065-1078.
18. Hohmann S (2002). Osmotic stress signaling and osmoadaptation in yeasts. Microbiology and Molecular Biology Reviews 66:300-372.
19. Hoog GS de (1993). Evolution of black yeasts: possible adaptation to the human host. Antonie van Leeuwenhoek 63:105-109.
20. Hoog GS de, Gerrits van den Ende AH (1992). Nutritional pattern and eco-physiology of Hortaea werneckii, agent of human tinea nigra. Antonie van Leeuwenhoek 62:321-329.
21. th edn. (Kreier J, Wakelin D, Cox F, eds). Hodder Arnold, U.K.:100-112.
22. Hoog GS de, Hermanides-Nijhof E (1977). Survey of black yeasts and allied fungi. Studies in Mycology 15:178-221.
23. Iwatsu TU, Udagawa S (1988). Hortaea werneckii isolated from sea-water. Japanese Journal of Medical Mycology 29:142-145.
24. Jacobson ES, Ikeda R (2005). Effect of melanization upon porosity of the cryptococcal cell wall. Medical Mycology 43:327-333.
25. Klipp E, Nordlander B, Krüger R, Gennemark P, Hohmann S (2005). Integrative model of the response of yeast to osmotic shock. Nature Biotechnolgy 23:975-982.
26. Kogej T, Gorbushina AA, 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. Mycology Research 110:713-724.
27. Kogej T, Gostinar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N (2006). Mycosporines in extremophilic fungi - novel complementary osmolytes? Environmental Chemistry 3:105-110.
28. 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. Applied and Environmental Microbiology 71:6600-6605.
29. 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 153:4261-4273.
30. Kogej T, Wheeler MH, Lanisnik Rizner T, Gunde-Cimerman N (2004). Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiology Letters 232:203-209.
31. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV (2002). Selection in the evolution of gene duplications. Genome Biology 3:0008.1-0008.9.
32. Lenassi M, Plemenitaš A (2007). Novel group VII histidine kinase HwHhk7B from the halophilic fungi Hortaea werneckii has a putative role in osmosensing. Current Genetics 51:393-405.
33. Lenassi M, Vaupotič T, Gunde-Cimerman N, Plemenitaš A (2007). The MAP kinase HwHog1 from the halophilic black yeast Hortaea werneckii: coping with stresses in solar salterns. Saline Systems 3:3 .
34. Li J, Steen H, Gygi SP (2003). Protein profiling with cleavable isotope-coded affinity tag (cICAT) reagents: the yeast salinity stress response. Molecular and Cellular Proteomics 2:1198-1204.
35. Liska AJ, Shevchenko A, Pick U, Katz A (2004). Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiology 136:2806-2817.
36. Mager WH, Siderius M (2002). Novel insights into the osmotic stress response of yeast. FEMS Yeast Research 2:251-257.
37. Mejanelle L, Lòpez JF, Gunde-Cimerman N, Grimalt JO (2001). Ergosterol biosynthesis in novel melanized fungi from hypersaline environments. Journal of Lipid Research 42:352-358.
38. Mok W, Barreto da Silva MS (1981). Occurrence of Exophiala werneckii on salted freshwater fish Osteoglossum bicirrhosum. Journal Food Technology 16:505-512.
39. Nemecek JC, Wuthrich M, Klein BS (2006). Global control of dimorphism and virulence in fungi. Science 312:583-588.
40. Norbeck J, Blomberg A (1997). Metabolic and regulatory changes associated with growth of Saccharomyces cerevisiae in 1.4 M NaCl. Evidence for osmotic induction of glycerol dissimilation via the dihydroxyacetone pathway. Journal of Biological Chemistry 272:5544-5554.
41. O'Rourke SM, Herskowitz I (2004). Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Molecular Biology of the Cell 15:532-542.
42. O'Rourke SM, Herskowitz I, O'Shea EK (2002). Yeast go the whole HOG for the hyperosmotic response. Trends in Genetics 18:405-412.
43. Oren A (1999). Bioenergetic aspects of halophilism. Microbiology and Molecular Biology Reviews 63:334-348.
44. Oren A (2002). Halophilic microorganisms and their environments. Kluwer, Dordrecht, the Netherlands.
45. Oren A, Gunde-Cimerman N (2007). Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiology Letters 269:1-10.
46. 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. Journal of Biological Chemistry 281:4638-4645.
47. Petrovic U (2006). Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Research 6:816-822.
48. Petrovic U, Gunde-Cimerman N, Plemenitaš A (2002). Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Molecular Microbiology 45:665-672.
49. Pfyffer G, Pfyffer BU, Rast DM (1986). The polyol pattern, chemotaxonomy, and phylogeny of the fungi. Sydowia 39:160-201.
50. Plemenitaš A, Gunde-Cimerman N (2005). Cellular reponses in the halophilic black yeast Hortaea weneckii to high environmental salinity. In: Adaptation to Life at High Salt Concentrations in Archea, Bacteria and Eukarya (Gunde-Cimerman N, Oren A, Plemenitaš A, eds). Springer, the Netherlands:455-470.
51. Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Ariño J (2000). The transcriptional response of yeast to saline stress. Journal of Biological Chemistry 275:17249-17255.
52. Prista C, Almagro A, Loureiro-Dias MC, Ramos J (1997). Physiological basis for the high salt tolerance of Debaryomyces hansenii.Applied and Environmental Microbiology 63:4005-4009.
53. Prista C, Loureiro-Dias MC, Montiel V, García R, Ramos J (2005). Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Research 5:693-701.
54. Proft M, Mas G, de Nadal E, Vendrell A, Noriega N, Struhl K, Posas F (2006). The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Molecular Cell 23:241-250.
55. Ramos J (1999). Contrasting salt tolerance mechanisms in Saccharomyces cerevisiae and Debaryomyces hansenii. In: Recent Research Developments in Microbiology (Pandalai SG, ed). Research Signpost, Trivandrum, India:377-390.
56. Ramos J (2005). Introducing Debaryomyces hansenii, a salt-loving yeast. In:, Adaptation to Life at High Salt Concentrations in Archea, Bacteria and Eukarya (Gunde-Cimerman N, Oren A, Plemenitaš A, eds). Springer, the Netherlands: 441-451.
57. Ruibal C, Platas G, Bills GF (2008). High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia 21:93-110.
58. Santos JL, Shiozaki K (2001). Fungal histidine kinases. Science Signal Transduction Knowledge,4 Sept: Re1.
59. Sheffer M, Fried A, Gottlieb H, Tietz A, Avron M (1986). Lipid composition of the plasma-membrane of the halotolerant alga Dunaliella salina. Biochimica et Biophysica Acta 857:165-172.
60. Silva-Graca M, Lucas C (2003). Physiological studies on long-term adaptation to salt stress in the extremely halotolerant yeast Candida versatilis CBS 4019 (syn. C. halophila). FEMS Yeast Research 3:247-260.
61. Sterflinger K, Hoog GS de, Haase G (1999). Phylogeny and ecology of meristematic ascomycetes. Studies in Mycology 43:5-22.
62. Tamas MJ, Rep M, Thevelein JM, Hohmann S (2000). Stimulation of the yeast high osmolarity glycerol (HOG) pathway: evidence for a signal generated by a change in turgor rather than by water stress. FEBS Letters 472:159-165.
63. Todaro FBA, Cavaliere A, Criseo G, Pernice L (1983). Gasophtalmus in black sea bream (Spodyliosoma cantharus) caused by Sarcinomyces crustaceus Lindner. Mycopathologia 81:95-97.
64. Turk M, Abramovic Z, Plemenitaš A, Gunde-Cimerman N (2007). Salt stress and plasma-membrane fluidity in selected extremophilic yeasts and yeast-like fungi. FEMS Yeast Research 7:550-557.
65. Turk M, Méjanelle L, Sentjurc 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 8:53-61.
66. 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 Microbiology Letters 216:193-199.
67. 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 Genetics and Biology 44:1109-1122.
68. Vaupotič T, Plemenitaš A (2007). Differential gene expression and Hog1 interaction with osmoresponsive genes in the extremely halotolerant black yeast Hortaea werneckii. BMC Genomics 8:280 .
69. Westfall PJ, Ballon DR, Thorner J (2004). When the stress of your environment makes you go HOG wild. Science 306:1511-1512.
70. Wolanin PM, Thomason PA, Stock JB (2002). Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biology 3:3013.
71. Wollenzien U, Hoog GS de, Krumbein WE, Urzì C (1995). On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Science of the Total Environment 167:287-294.
72. Yale J, Bohnert HJ (2001). Transcript expression in Saccharomyces cerevisiae at high salinity. Journal of Biological Chemistry 276:15996-16007.
73. Yancey PH (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology 208:2819-2830.
74. Zalar P, Hoog GS de, Gunde-Cimerman N (1999). Ecology of halotolerant dothideaceous black yeasts. Studies in Mycology 43:38-48.
75. Zalar P, Kocuvan MA, Plemenitaš A, Gunde-Cimerman N (2005). Halophilic black yeast colonize wood immersed in hypersaline water. Botanica Marina 48:323-326.