1887

Abstract

The food spoilage yeasts and have been proposed to resist weak-acid preservative stress by different means; by limiting influx of preservative combined with its catabolism, by active extrusion of the preservative weak-acid anion and H. Measurement of H extrusion by exponential-phase cells suggest that, in common with , this yeast uses a plasma membrane H-ATPase to expel H when challenged by weak-acid preservative (benzoic acid). Simultaneous measurement of net H and K fluxes showed that net K influx accompanies net H efflux during acute benzoic acid stress. Such ionic coupling is known for in short-term preservative stress. Both yeasts significantly accumulated K on long-term exposure to benzoic acid. Analysis of K transporter mutants revealed that loss of the high affinity K uptake system confers sensitivity to growth in preservative. The results suggest that cation accumulation is an important factor in adaptation to weak-acid preservatives by spoilage yeasts and that and share hitherto unsuspected adaptive responses at the level of plasma membrane ion transport.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27502-0
2005-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/6/mic1511995.html?itemId=/content/journal/micro/10.1099/mic.0.27502-0&mimeType=html&fmt=ahah

References

  1. Aiking H., Sterkenberg A., Tempest D. W. 1977; Influence of simple growth limitation and dilution rate on the phosphorylation efficiency and cytochrome content of mitochondria of Candida utilis NCYC 321. Arch Microbiol 108:117–124
    [Google Scholar]
  2. Bowman B. J., Allen K. E., Slayman C. W. 1983; Vanadate-resistant mutants of Neurospora crassa are deficient in a high-affinity phosphate transport system. J Bacteriol 153:292–296
    [Google Scholar]
  3. Boxman A. W., Theuvenet A. P. R., Peters P. H. J., Dobbelmann J., Borst-Pauwels G. W. F. H. 1985; Regulation of 86Rb influx during accumulation of Rb+ or K+ in yeast. Biochim Biophys Acta 814:50–56 [CrossRef]
    [Google Scholar]
  4. Brooker R. J., Slayman C. W. 1982; Inhibition of the plasma membrane H+-ATPase ofNeurospora crassa by N-ethylmaleimide. J Biol Chem 257:12051–12055
    [Google Scholar]
  5. Cole M. B., Kiernan M. H. J. 1987; Effects of weak acids and external pH on the intracellular pH of Zygosaccharomyces bailii and its implications in weak-acid resistance. Yeast 3:23–32 [CrossRef]
    [Google Scholar]
  6. Davies J. M., Brownlee C., Jennings D. H. 1990; Electrophysiological evidence for an electrogenic proton pump and proton symport of glucose in the marine fungus Dendryphiella salina . J Exp Bot 41:449–456 [CrossRef]
    [Google Scholar]
  7. Fairman C., Zhou X.-L., Kung C. 1999; Potassium uptake through the TOK1 channel in budding yeast. J Membr Biol 168:149–157 [CrossRef]
    [Google Scholar]
  8. Haro R., Rodríguez-Navarro A. 2002; Molecular analysis of the mechanism of potassium uptake through the TRK1 transporter of Saccharomyces cerevisiae. Biochim Biophys Acta 1564114–122 [CrossRef]
    [Google Scholar]
  9. Holyoak C. D., Stratford M., McMullin Z., Cole M. B., Crimmins K., Brown A. J. P., Coote P. J. 1996; Activity of the plasma membrane H+-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol 62:3158–3164
    [Google Scholar]
  10. Holyoak C. D., Bracey D., Piper P. W., Kuchler K., Coote P. J. 1999; The Saccharomyces cerevisiae weak acid-inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy-dependent mechanism. J Bacteriol 181:4644–4652
    [Google Scholar]
  11. Jones R. P., Gadd G. M. 1990; Ionic nutrition of yeast – physiological mechanisms involved and implications for biotechnology. Enzyme Microb Technol 12:402–418 [CrossRef]
    [Google Scholar]
  12. Ketchum K. A., Joiner W. J., Sellers A. J., Kaczmarek L. K., Goldstein S. A. 1995; A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376:690–695 [CrossRef]
    [Google Scholar]
  13. Krebs H. A., Wiggins D., Stubbs M., Sols A., Bedoya F. 1983; Studies on the mechanism of the antifungal action of benzoate. Biochem J 214:657–663
    [Google Scholar]
  14. Madrid R., Gómez M. J., Ramos J., Rodríguez-Navarro A. 1998; Ectopic potassium uptake in trk1trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. J Biol Chem 273:14838–14844 [CrossRef]
    [Google Scholar]
  15. Mollapour M., Piper P. W. 2001; The ZbYME2 gene from the food spoilage yeast Zygosaccharomyces bailii confers not only YME2 functions in Saccharomyces cerevisiae but also the capacity for catabolism of sorbate and benzoate, two major weak organic acid preservatives. Mol Microbiol 42:919–930 [CrossRef]
    [Google Scholar]
  16. Mollapour M., Fong D. N., Balakrishnan K., Harris N., Thompson S., Schuller C., Kuchler K., Piper P. W. 2004; Screening the yeast deletant mutant collection for hypersensitivity and hyper-resistance to sorbate, a weak organic acid food preservative. Yeast 21:927–946 [CrossRef]
    [Google Scholar]
  17. Nakamura T., Liu Y., Hirata D. H., Namba H., Harada S.-I., Hirokawa T., Miyakawa T. 1993; Protein phosphatase type 2B (calcineurin)-mediated FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J 12:4063–4071
    [Google Scholar]
  18. Newman I. A. 2001; Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterise transporter function. Plant Cell Environ 24:1–14 [CrossRef]
    [Google Scholar]
  19. Northrop F. D., Ljubojevic S., Davies J. M. 1997; Influence of Na+ and anions on the dimorphic transition of Candida albicans. Microbiology 143:3757–3765 [CrossRef]
    [Google Scholar]
  20. Nuñez M., Peña R. M., Herrero C., García S. 2000; Determination of six metals in Galician red wines (in Northwestern Spain) by capillary electrophoresis. J AOAC Int 83:183–188
    [Google Scholar]
  21. Piper P. W. 1999; Yeast superoxide dismutase mutants reveal a prooxidant action of weak organic acid food preservatives. Free Radic Biol Med 27:1219–1227 [CrossRef]
    [Google Scholar]
  22. Piper P. W., Thompson S., Pandjaitan R., Holyoak C., Egner R., Coote P., Kuchler K, Mahé Y., Mühlbauer M. 1998; The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J 17:4257–4265 [CrossRef]
    [Google Scholar]
  23. Piper P., Ortiz Calderon C., Hatzixanthis K., Mollapur M. 2001; Weak acid adaptation; the stress response that confers yeasts with resistance to organic acid preservatives. Microbiology 147:2635–2642
    [Google Scholar]
  24. Ramos J., Alijo R., Haro R., Rodríguez-Navarro A. 1994; TRK2 is not a low-affinity transporter in Saccharomyces cerevisiae. J Bacteriol 176:249–252
    [Google Scholar]
  25. Rodrigues F., Ludovico P., Sousa M. J., Steensma H. Y., Côrte-Real M., Leão M. 2003; The spoilage yeast Zygosaccharomyces bailii forms mitotic spores: a screening method for haploidization. Appl Environ Microbiol 69:649–653 [CrossRef]
    [Google Scholar]
  26. Rodríguez-Navarro A., Ramos J. 1984; Dual system for potassium transport in Saccharomyces cerevisiae. J Bacteriol 159:940–945
    [Google Scholar]
  27. Ryan J. P., Ryan H. 1972; The role of intracellular pH in the regulation of cation exchanges in yeast. Biochem J 128:139–146
    [Google Scholar]
  28. Ryan H., Ryan J. P., O'Connor W. H. 1971; The effect of diffusible acids on potassium ion uptake by yeast. Biochem J 125:1081–1084
    [Google Scholar]
  29. Scarborough G. A., Addison R. 1984; On the subunit composition of the Neurospora plasma membrane H+-ATPase. J Biol Chem 259:9109–9114
    [Google Scholar]
  30. Serrano R. 1980; Effect of inhibitors on the proton pump of respiratory deficient yeast. Eur J Biochem 105:419–424 [CrossRef]
    [Google Scholar]
  31. Shabala S., Newman I. 1999; Light-induced changes in hydrogen, calcium, potassium and chloride ion fluxes and concentrations from the mesophyll and epidermal tissues of bean leaves. Plant Physiol 119:1115–1124 [CrossRef]
    [Google Scholar]
  32. Shabala L., Shabala S., Ross T., McMeekin T. 2001a; Membrane transport activity and ultradian ion flux oscillations associated with cell cycle of Thraustochytrium sp. Aust J Plant Physiol 28:87–99
    [Google Scholar]
  33. Shabala L., Ross T., Newman I., McMeekin T., Shabala S. 2001b; Measurements of net fluxes and extracellular changes of H+,Ca2+, K+ and in Escherichia coli using ion-selective microelectrodes. J Microbiol Methods 46:119–129 [CrossRef]
    [Google Scholar]
  34. Shabala L., Budde B., Ross T., Siegumfeldt H., Jakobsen M., McMeekin T. 2002; Responses of Listeria monocytogenes to acid stress and glucose availability revealed by a novel combination of fluorescence microscopy and microelectrode ion-selective techniques. Appl Environ Microbiol 68:1794–1802 [CrossRef]
    [Google Scholar]
  35. Stratford M., Anslow P. A. 1998; Evidence that sorbic acid does not inhibit yeast as a classic ‘weak acid preservative’. Lett Appl Microbiol 27:203–206 [CrossRef]
    [Google Scholar]
  36. Thomas D. S., Davenport R. 1985; Zygosaccharomyces bailii – a profile of characteristics and spoilage activities. Food Microbiol 2:157–169 [CrossRef]
    [Google Scholar]
  37. Viegas C. A., Sa-Correia I. 1991; Activation of plasma membrane ATPase of Saccharomyces cerevisiae by octanoic acid. J Gen Microbiol 137:645–651 [CrossRef]
    [Google Scholar]
  38. Warnke J., Slayman C. L. 1980; Metabolic modulation of stoichiometry of a proton pump. Biochim Biophys Acta 591:224–233 [CrossRef]
    [Google Scholar]
  39. Warth A. D. 1989; Transport of benzoic and propanoic acids by Zygosaccharomyces bailii. J Gen Microbiol 135:1383–1390
    [Google Scholar]
  40. Yenush L., Mulet J. M., Arino J., Serrano R. 2002; The Ppz protein phosphatases are key regulators of K+ and pH homeostasis: implications for salt tolerance, cell wall integrity and cell cycle progression. EMBO J 21:920–929 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27502-0
Loading
/content/journal/micro/10.1099/mic.0.27502-0
Loading

Data & Media loading...

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