Abstract
The non-pathogenic, dimorphic, ascomycetous yeast Arxula adeninivorans LS3 is halotolerant. It can grow in a minimal medium containing up to 20% NaCl. The growth parameters are only weakly influenced by 10% NaCl. However, NaCl in a concentration higher than 10% causes a decrease in the specific growth rate, a longer adaptation phase and a lower cell count in the stationary growth phase. Concentrations of glycerol and trehalose, which differed 100-fold in magnitude in a salt free medium, are also influenced differently by salt. NaCl induces accumulation of intracellular glycerol in exponentially growing cells but a reduced concentration of intracellular trehalose in stationary cells. Transcripts of the genes ARFC3, encoding a component of the replication factor C, and GAA, encoding a secretory glucoamylase, can be detected only in cells cultured in media with NaCl concentrations below 10%. Furthermore, NaCl in high concentration reduces the level of secreted proteins including glucoamylase end invertase.
Similar content being viewed by others
References
Adler L & Gustafsson L (1980) Polyhydric alcohol production and intracellular amino acid pool in relation to halotolerance of the yeast Debaryomyces hansenii. Arch. Microbiol. 124: 123–130
Adler L, Blomberg A & Nilsson A (1985) Glycerol metabolism and osmoregulation in the salt-tolerant yeast Debaryomyces hansenii. J. Bacteriol. 162: 300–306
Araujo PS, Panek AC, Ferreira R & Panek AD (1989) Determination of trehalose in biological samples by simple and stable trehalase preparation. Anal. Biochem. 176: 432–436
Attfield PV (1987) Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett. 225: 259–263
Blomberg A & Adler L (1989) Roles of glycerol and glycerol-3-phosphate dehydrogenase (NADC) in acquired osmotolerance of Saccharomyces cerevisiae. J. Bacteriol. 171: 1087–1092
Blomberg A & Adler L (1992) Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33: 145–212
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254
Brown AD & Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J. Gen Microbiol. 72: 589–591
Brown AD (1978) Compatible solutes and extreme water stress in eukaryotic microorganisms. Adv. Microbiol. Physiol. 17: 181–242
Bui DM, Kunze I, Förster S, Wartmann T, Horstmann C, Manteuffel R & Kunze G (1996a) Cloning and expression of an Arxula adeninivorans glucoamylase gene in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 44: 610–619
Bui DM, Kunze I, Horstmann C, Schmidt T, Breunig KD & Kunze G (1996b) Expression of the Arxula adeninivorans glucoamylase gene in Kluyveromyces lactis. Appl. Microbiol. Biotechnol. 45: 102–106
Buttner R, Bode R & Birnbaum D (1987) Purification and characterization of the extracellular glucoamylase from the yeast Trichosporon adeninovorans. J. Basic Microbiol. 27: 299–308
Crowe JH, Crowe LM & Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: The role of trehalose. Science 223: 701–703
Davis E, Larkins BA & Knight RH (1972) Polyribosomes from peas. An improved method for their isolation in the absence of ribonuclease inhibitors. Plant Physiol. 50: 581–584
Edgley M & Brown AD (1983) Yeast water relations: physiological changes induced by solute stress in Saccaromyces rouxii. J.Gen. Microbiol. 129: 3453–3463
Garcia MJ, Rios G, Ali R, Belles JM & Serrano R (1997) Comparative physiology of salt tolerance in Candida tropicalis and Saccharomyces cerevisiae. Microbiology 143: 1125–1131
Gienow U, Kunze G, Schauer F, Bode R & Hofemeister J (1990) The yeast genus Trichosporon spec. LS3: molecular characterization of genomic complexity. Zbl. Mikrobiol. 145: 3–12
Gustafsson L & Norkrans B (1976) On the mechanism of salt tolerance: production of glycerol and heat during growth of Debaryomyces hansenii Arch. Microbiol. 110: 177–183
Haro R, Garciadeblas B & Rodriguez-Navarro A (1991) A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett. 291: 189–191
Hohmann S (1997) Shaping up: the response of yeast to osmotic stress. In: Hohmann S & Mager WH (Eds) Yeast stress responses (pp 101–145), RG Landes, Austin, TX
Hottinger T, Boller T & Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett. 220: 113–115
Hounda C-G, Vincent Brandt E, Thevelein J, Hohmann S & Prior BA (1998) Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. Microbiology 144: 671–680
Kunze G & Kunze I (1994a) Characterization of Arxula adeninivorans strains from different habitats. Antonie van Leeuwenhoek 65: 29–34
Kunze G & Kunze I (1994b) Comparative study of morphological characteristics and secretory invertase activities of Arxula adeninivorans. Microbiol. Europe 2: 24–28
Laemmli UK (1970) Cleavage of structural protein during assembly of the head of bacteriophage T4. Nature (London) 227: 680–685
Lages F & Lucas C (1995) Characterization of a glycerol/HC symport in the halotolerant yeast Pichia sorbitophila Yeast 11: 111–119
Larsson C & Gustafsson L (1987) Glycerol production relation to the ATP pool and heat production rate of the yeasts Debaryomyces hansenii and Saccharomyces cerevisiae during salt stress. Arch. Microbiol. 147: 358–363
Larsson C & Gustafsson L (1993) The role of physiological state in osmotolerance of the salt-tolerant yeast Debaryormyces hansenii. Can. J. Microbiol. 39: 603–609
Lillie SH & Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: Responses to nutrient limitation. J. Bacteriol. 143: 1384–1394
Londesborough J & Vuorio O (1991) Trehalose-6-phosphate synthase/ phosphatase complex from baker's yeast: purification of a proteolytically activated form. J. Gen. Microbiol. 137: 323–830
Middelhoven WJ, Hoogkamer-Te Niet MC & Kreger van Rij NJW (1984) Trichosporon adeninvorans sp. nov., a yeast species utilizing adenine, xanthine, uric acid, putrescine and primary nalkylamines as the sole source of carbon, nitrogen and energy.Antonie van Leeuwenhoek 50: 369–387
Middelhoven WJ, de Jonge IM & de Winter M (1991) Arxula adeninivorans a yeast assimilating many nitrogenous and aromatic compounds. Antonie van Leeuwenhoek 59: 129–137
Middelhoven WJ, Coenen A, Kraakman B & Gelpke MDS (1992) Degradation of some phenols and hydroxybenzoates by the imperfect ascomycetous yeasts Candida parapsilosis and Arxula adeninivorans: evidence for an operative gentisate pathway. Antonie van Leeuwenhoek 62: 181–187
Neves ML, Oliveira RP & Lucas CM (1997) Metabolic flux response to salt-induced stress in the halotolerant yeast Debaryomyces hansenii. Microbiology 143: 1133–1139
Prista C, Almagro A, Loureiro-Dias MC & Ramos J (1997) Physiological basis for the high salt tolerance of Dabaryomyces hansenii. Appl. Environ. Microbiol. 63: 4005–4009
Rausch T, Kirsch M, Low R, Lehr A, Viereck R & Zhigang A (1996) Salt stress responses of higher plants: the role of proton pumps and Na+/HC+-antiporters. J. Plant Physiol. 148: 425–433
Rösel H & Kunze G (1995) Cloning and characterization of a TEF gene for elongation factor 1α from the yeast Arxula adeninivorans. Curr. Genet. 28: 360–366
Sambrook J, Fritsch EF & Maniatis T (1989) Molecular cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, New York
Stoltenburg R, Wartmann T, Kunze I & Kunze G (1995) Reliable method to prepare RNA from free and membrane-bound polysomes from different yeast species. Bio/Technology 18: 564–568
Stoltenburg R, Lösche O, Klapach G & Kunze G (1999) Molecular cloning and expression of the ARFC3 gene, a component of the replication factor C from the salt-tolerant, dimorphic yeast Arxula adeninivorans. Curr. Genet. 35: 8–13
Tanaka A, Ohnishi N & Fukui S (1967). Studies on the formation of vitamins and their function in hydrocarbon fermentation. Production of vitamin B by Candida albicans in hydrocarbon medium. J. Ferment. Technol. 45: 617–623
Thevelein JM (1988) Regulation of trehalase activity by phosphorylation-dephosphorylation during developmental transitions in fungi. Exp. Mycol. 12: 1–12
Van der Walt JP, Smith MT & Yamada Y (1990) Arxula gen. nov. (Candidaceae), a new anamorphic, arthroconidial yeast genus. Antonie van Leeuwenhoek 57: 59–61
Wartmann T, Kunze I, Bui MD, Manteuffel R & Kunze G (1995a) Comparative biochemical, genetical and immunological studies of glucoamylase producing Arxula adeninivorans strain. Microbiol. Res. 150: 113–120
Wartmann T, Krüger A, Adler K, Bui MD, Kunze I & Kunze G (1995b) Temperature-dependent dimorphism of the yeast Arxula adeninivorans LS3. Antonie van Leeuwenhoek 68: 215–223
Wartmann T, Erdmann J, Kunze I & Kunze G (2000) Morphologyrelated effects on gene expression and protein accumulation of the yeast Arxula adeninivorans LS3.
Yagi T (1988) Intracellular levels of glycerol necessary for initiation of growth under salt-stressed conditions in a salt-tolerant yeast, Zygosaccharomyces rouxii. FEMS Microbiol. Lett. 49: 25–30
Yagi T & Tada K (1988) Isolation and characterization of saltsensitive mutants of a salt-tolerant yeast Zygosaccharomyces rouxii. FEMS Microbiol. Lett. 49: 317–321
Yagi T (1991) Effects of increases and decreases in the external salinity on the intracellular glycerol and inorganic ion content in the salt-tolerant yeast. Microbios 68: 109–117
Yagi T (1992) Regulation of intracellular osmotic pressure during the initial stages of salt stress in a salt-tolerant yeast, Zygosaccharomyces rouxii. Microbios 70: 93–102
Yagi T & Nishi T (1993) Regulation of intracellular osmotic pressure and changes in intracellular proteins during the initial stages of salt stress in Zygosaccharomyces strains exhibiting differences in salt-tolerance. Microbios 74: 155–166
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yang, XX., Wartmann, T., Stoltenburg, R. et al. Halotolerance of the yeast Arxula adeninivorans LS3. Antonie Van Leeuwenhoek 77, 303–311 (2000). https://doi.org/10.1023/A:1002636606282
Issue Date:
DOI: https://doi.org/10.1023/A:1002636606282