Abstract
Molecular studies on halophilic adaptations have focused on prokaryotic microorganisms due to a lack of known appropriate eukaryotic halophilic microorganisms. However, the black yeast Hortaea werneckii has been identified as the dominant fungal species in hypersaline waters on three continents. It represents a new model organism for studying the mechanisms of salt tolerance in eukaryotes. Ultrastructural studies of the H. werneckii cell wall have shown that it synthesizes dihydroxynaphthalene (DHN) melanin under both saline and non-saline growth conditions. However, melanin granules in the cell walls are organized in a salt-dependent way, implying the potential osmoprotectant role of melanin. At the level of membrane structure, H. werneckii maintains a sterol-to-phospholipid ratio significantly lower than the salt-sensitive Saccharomyces cerevisiae. Accordingly, membranes of H. werneckii are more fluid over a wide range of NaCl concentrations, indicating high intrinsic salt stress tolerance. Even H. werneckii grown in high NaCl concentrations maintains very low intracellular amounts of potassium and sodium, demonstrating the sodium-excluder character of this organism. The salt-dependent expressions of two HwENA genes suggest roles for them in the adaptation to changing salt concentrations. The high similarity of these ENA ATPases to other fungal ENA ATPases involved in Na+/K+ transport indicates their potential importance in H. werneckii ion homeostasis. Glycerol is the main compatible solute which accumulates in the cytoplasm of H. werneckii at high salinity, although it seems that mycosporines may also act as supplementary compatible solutes. Salt dependent increase in glycerol synthesis is supported by the identification of two copies of a gene putatively coding for glycerol-3-phosphate-dehydrogenase. Expression of only one of these genes is salt dependent.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Almagro A, Prista C, Quintas C, Madeira Lopes A, Ramos J, Loureiro-Dias MC (2000) Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int J Food Microbiol 56:191–197
Almagro A, Prista C, Benito B, Loureiro-Dias MC, Ramos J (2001) Cloning and expression of two genes coding for sodium pumps in the salt-tolerant yeast Debaryomyces hansenii. J Bacteriol 183(10):3251–3255
Andre L, Nillsson A, Adler L (1988) The role of glycerol in osmotolerance of the yeast Debaromyces hansenii. J Gen Microbiol 134:669–677
Andreishcheva EN, Isakova EP, Sidorov NN, Abramova NB, Ushakova NA, Shaposhnikov GL, Soares MIM, Zvyagilskaya RA (1999) Adaptation to salt stress in a salt-tolerant strain of the yeast Yarrowia lipolytica. Biochemistry 64(9):1061–1067 (Moscow)
Andrews S, Pitt JI (1987) Further studies on the water relations of xerophilic fungi, including some halophiles. J Gen Microbiol 133:233–238
Bandaranayake WM (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15(2):159–172
Banuelos MA, Rodriguez-Navarro A (1998) P-type ATPases mediate sodium and potassium effluxes in Schwanniomyces occidentalis. J Biol Chem 273(3):1640–1646
Bell AA, Wheeler MH (1986) Biosynthesis and functions of fungal melanins. Annu Rev Phytopathol 24:411–451
Benito B, Garciadeblas B, Rodriguez-Navarro A (2002) Potassium- or sodium-efflux ATPase, a key enzyme in the evolution of fungi. Microbiology 148(Pt 4):933–941
Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212
Blomberg A (2000) Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiol Lett 182(1):1–8
Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244(2):229–234
Elliot ML, Henson JM (2001) Effect of osmotic stress on growth of Gaeumannomyces graminis strains differing in hyphal pigmentation. Mycologia 93(4):617–625
Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:272–328
Garciadeblas B, Rubio F, Quintero FJ, Banuelos MA, Haro R, Rodriguez-Navarro A (1993) Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol Gen Genet 236(2–3):363–368
Gorbushina AA, Krumbein WE, Hamann CH, Panina LK, Soukharjevski SM, Wollenzien U (1993) Role of black fungi in color change and biodeterioration of antique marbles. Geomicrobiol J 11:205–211
Göttlich E, de Hoog GS, 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
Gunde-Cimerman N, Frisvad JC, Zalar P, Plemenitaš A (2005) Halotolerant and halophilic fungi. Oxford & IBH Publishing Co. Pvt. Ltd.
Gunde-Cimerman N, Zalar P, de Hoog GS, Plemenitaš A (2000) Hypersaline waters in salterns – natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32(3):235–240
Holker U, Bend J, Pracht R, Tetsch L, Muller T, Hofer M, de Hoog GS (2004) Hortaea acidophila, a new acid-tolerant black yeast from lignite. Anton Van Leeuwen 86(4):287–294
de Hoog GS (1993) Evolution of black yeasts: possible adaptation to the human host. Anton Van Leeuwen 63:105–109
de Hoog G, Hermanides-Nijhof E (1977) Survey of black yeasts and allied fungi. Stud Mycol 15:178–221
de Hoog GS, Gerrits van den Ende AHG (1992) Nutritional pattern and eco-physiology of Hortaea werneckii, agent of human tinea nigra. Anton Van Leeuwen 62:321–329
de Hoog GS, Guého E (1998) Agents of white piedra, black piedra and tinea nigra. In: Asello L, Hay RJ (eds) Topley and Wilsons microbiology and microbial infections, 3rd edn., vol 4. Arnold, London, pp 1–15
de Hoog GS, Zalar P, Urzi C, de Leo F, Yurlova NA, Sterflinger K (1999) Relationships of dothideaceous black yeasts and meristematic fungi based on 5.8S and ITS2 rDNA sequence comparison. Stud Mycol 43:33–40
Hosono K (1992) Effect of salt stress on lipid composition and membrane fluidity of the salt-tolerant yeast Zygosaccharomyces rouxii. J Gen Microbiol 138:91–96
Iwatsu T, Udagawa S (1988) Hortaea werneckii isolated from sea-water. Jpn J Med Mycol 29(2):142–145
Khaware RK, Koul A, Prasad R (1995) High membrane fluidity is related to NaCl stress in Candida membranefaciens. Biochem Mol Biol Int 35(4):875–880
Kogej T (2006) Physiological adaptations of halophilic black yeast Hortaea werneckii to growth at saline conditions on the levels of cell wall and accumulation of compatible solutes. Doctoral Thesis, Ljubljana, 198 pp
Kogej T, Gostinčar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N (2006) Mycosporines in extremophilic fungi – novel complementary osmolytes? Environ Chem 3(2):105–110
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(11):6600–6605
Kogej T, Wheeler MH, Lanišnik Rižner T, Gunde-Cimerman N (2004) Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiol Lett 232(2):203–209
Krumbein WE, Gorbushina AA, Sterflinger K, Haroska U, Kunert U, Drewello R, Weißmann R (1996) Biodeterioration of historical window panels of the former Cistercian Monastery church of Haina (Hessen, Germany). DECHEMA Monographs 133:417–424
Leach CM (1965) Ultraviolet-absorbing substances associated with light-induced sporulation in fungi. Can J Bot 43:185–200
Libkind D, Perez P, Sommaruga R, Dieguez Mdel C, Ferraro M, Brizzio S, Zagarese H, van Broock M (2004) Constitutive and UV-inducible synthesis of photoprotective compounds (carotenoids and mycosporines) by freshwater yeasts. Photochem Photobiol Sci 3(3):281–286
Mok WYC, Barreto da Silva MS (1981) Occurrence of Exophiala werneckii on salted freshwater fish Osteoglossum bicirrhosum. J Food Technol 16:505–512
Nevoigt E, Stahl U (1997) Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 21(3):231–241
Nienow JA, Friedman EI (1993) Terrestrial lithophytic (rock) communities. In: Friedmann EI (ed) Antarctic Microbiology (Wiley Series in Ecological and Applied Microbiology), pp 342–412. Wiley-Liss, 644 pp
Oren A (1997) Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol J 14:231–240
Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63(2):334–348
Petrovič U, Gunde-Cimerman N, Plemenitaš A (1999) Salt stress affects sterol biosynthesis in the halophilic black yeast Hortaea werneckii. FEMS Microbiol Lett 180(2):325–330
Petrovič U, Gunde-Cimerman N, Plemenitaš A (2002) Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Mol Microbiol 45(3):665–672
Pfyffer GE, Pfyffer BU, Rast DM (1986) The polyol pattern, chemotaxonomy, and phylogeny of the fungi. Sydowia 39:160–201
Plemenitaš A, Gunde-Cimerman N (2005) Cellular reponses in the halophilic black yeast Hortaea weneckii to high environmental salinity. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archea, Bacteria and Eukarya. Springer, Dordrecht, The Netherlands, pp 455–470
Prista C, Loureiro-Dias MC, Montiel V, García R, Ramos J (2005) Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res 5:693–701
Ramos J (1999) Contrasting salt tolerance mechanisms in Saccharomyces cerevisiae and Debaryomyces hansenii. In: Pandalai SG (ed) Recent research developments in microbiology, vol 3. Research Signpost, Trivandrum, India, pp 377–390
Ramos J (2005) Introducing Debaryomyces hansenii, a salt-loving yeast. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archea, Bacteria and Eukarya. Springer, Dordrecht, The Netherlands, pp 441–451
Russell NJ (1989a) Adaptive modifications in membranes of halotolerant and halophilic microorganisms. J Bioenerg Biomembr 21(1):93–113
Russell NJ (1989b) Structural and functional role of lipids. In: Ratledge C, Wilkinson SG (eds) Microbial lipids. Academic Press, New York, pp 279–349
Russell NJ, Evans, RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28(2):255–261
Sharma SC, Raj D, Forouzandeh M, Bansal MP (1996) Salt-induced changes in lipid composition and ethanol tolerance in Saccharomyces cerevisiae. Appl Biochem Biotechnol 56(2):189–195
Silva-Graça 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 Res 3(3):247–260
Slaninova I, Sestak S, Svoboda A, Farkas V (2000) Cell wall and cytoskeleton reorganization as the response to hyperosmotic shock in Saccharomyces cerevisiae. Arch Microbiol 173(4):245–252
Staley JT, Palmer F, Adams JB (1982) Microcolonial fungi: common inhabitants on desert rocks? Science 215:1093–1095
Sterflinger K, de Hoog GS, Haase G (1999) Phylogeny and ecology of meristematic ascomycetes. Stud Mycol 43:5–22
Todaro F, Berdar A, Cavaliere A, Criseo G, Pernice L (1983) Gasophtalmus in black sea bream (Spodyliosoma cantharus) caused by Sarcynomyces crustaceus Lindner. Mycopathologia 81:95–97
Trione EJ, Leach CM, Mutch JT (1966) Sporogenic substances isolated from fungi. Nature 212:163–164
Tunblad-Johansson I, Adler L (1987) Effect of sodium chloride concentration on phospholipid fatty acid composition of yeasts differing in osmotolerance. FEMS Microbiol Lett 43:275–278
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(2):193–199
Turk M, Mejanelle 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(1):53–61
Watanabe Y, Iwaki T, Shimono Y, Ichimiya A, Nagaoka Y, Tamai Y (1999) Characterization of the Na+-ATPase gene (ZENA1) from the salt-tolerant yeast Zygosaccharomyces rouxii. J Biosci Bioeng 88(2):136–142
Wollenzien U, de Hoog GS, Krumbein WE, Urzì C (1995) On the isolation of microcolonial fungi occurring on and in marble and other calcareous rocks. Sci Tot Env 167:287–294
Yoshikawa S, Mitsui N, Chikara KI, Hashimoto H, Shimosaka M, Okazaki M (1995) Effect of salt stress on plasma membrane permeability and lipid saturation in the salt-tolerant yeast Zygosaccharomyces rouxii. J Ferment Bioener 80(2):131–135
Zalar P, de Hoog GS, Gunde-Cimerman N (1999) Ecology of halotolerant dothideaceous black yeasts. Stud Mycol 43:38–48
Zalar P, Kocuvan MA, Plemenitaš A, Gunde-Cimerman N (2005) Halophilic black yeast colonize wood immersed in hypersaline water. Bot Mar 48:323–326
Zhdanova NN, Pokhodenko VD (1973) The possible participation of a melanin pigment in the protection of the fungus cell from desiccation. Microbiology 42:753–757
Zhdanova NN, Borisyuk LG, Artzatbanov VY (1990) Ocurrence of the K-type of life strategy in some melanin-containing fungi under experimental conditions. Folia Microbiol 35:423–430
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2006 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Gunde-Cimerman, N., Plemenitaš, A. (2006). Ecology and molecular adaptations of the halophilic black yeast Hortaea werneckii . In: Amils, R., Ellis-Evans, C., Hinghofer-Szalkay, H. (eds) Life in Extreme Environments. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6285-8_11
Download citation
DOI: https://doi.org/10.1007/978-1-4020-6285-8_11
Received:
Accepted:
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-6284-1
Online ISBN: 978-1-4020-6285-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)