Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives

References

1. Arneborg N., Jesperson L., Jakobsen M. 2000; Individual cells of Saccharomyces cerevisiae and Zygosaccharomyces bailii exhibit different short-term intracellular pH responses to acetic acid. Arch Microbiol 174:125–128 [CrossRef]
   [Google Scholar]
2. Bauer B. E., Wolfger H., Kuchler K. 1999; Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim Biophys Acta 1461217–236 [CrossRef]
   [Google Scholar]
3. Bracey D., Holyoak C. D., Coote P. J. 1998; Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae : is growth inhibition dependent on reduced intracellular pH?. J Appl Microbiol 85:1056–1066 [CrossRef]
   [Google Scholar]
4. Casal M., Cardoso H., Leão C. 1996; Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae . Microbiology 142:1385–1390 [CrossRef]
   [Google Scholar]
5. Cheng L., Piper P. W. 1994; Weak acid preservatives block the heat shock response and heat-shock-element-directed lacZ expression of low pH Saccharomyces cerevisiae cultures, an inhibitory action partially relieved by respiratory deficiency. Microbiology 140:1085–1096 [CrossRef]
   [Google Scholar]
6. Cheng L., Moghraby J., Piper P. W. 1999; Weak organic acid treatment causes a trehalose accumulation in low-pH cultures of Saccharomyces cerevisiae , not displayed by the more preservative-resistant Zygosaccharomyces bailii . FEMS Microbiol Lett 170:89–95 [CrossRef]
   [Google Scholar]
7. Cole M. B. 1987 The effect of weak acids and pH on Zygosaccharomyces bailii PhD thesis University of East Anglia;
   [Google Scholar]
8. Deak T. 1991; Food borne yeasts. Adv Appl Microbiol 36:179–278
   [Google Scholar]
9. De Nobel J. G., Barnett J. A. 1991; Passage of molecules through yeast cell walls: a brief essay-review. Yeast 7:313–323 [CrossRef]
   [Google Scholar]
10. Fleet G. 1992; Spoilage yeasts. Crit Rev Biotechnol 12:1–44 [CrossRef]
    [Google Scholar]
11. Henriques M., Quintas C., Loureiro-Dias M. C. 1997; Extrusion of benzoic acid in Saccharomyces cerevisiae by an energy-dependent mechanism. Microbiology 143:1877–1883 [CrossRef]
    [Google Scholar]
12. Holyoak C. D., Stratford M., McMullin Z., Cole M. B., Crimmins K., Brown A. J., 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]
13. 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]
14. Holyoak C. D., Thompson S., Ortiz Calderon C., Hatzixanthis K., Bauer B., Kuchler K., Piper P. W., Coote P. J. 2000; Loss of Cmk1 Ca²⁺/calmodulin-dependent protein kinase in yeast results in constitutive weak organic acid resistance, associated with a posttranscriptional activation of the Pdr12 ATP-binding cassette transporter. Mol Microbiol 37:595–605
    [Google Scholar]
15. Kalathenos P., Sutherland J. P., Roberts T. A. 1995; Resistance of some wine spoilage yeasts to combinations of ethanol and acids present in wine. J Appl Bacteriol 78:245–250 [CrossRef]
    [Google Scholar]
16. 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]
17. Lawson L. D. 1996; The composition and chemistry of garlic cloves and processed garlic. In Garlic. The Science and Therapeutic Application of Allium sativum L. and Related Species pp 37–107 Edited by Koch H. P., Lawson L. D. Baltimore: Williams & Wilkins;
    [Google Scholar]
18. Leonhard K., Guiard B., Pellecchia G., Tzagoloff A., Neupert W., Langer T. 2000; Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol Cell 5:629–638 [CrossRef]
    [Google Scholar]
19. Martinez-Pastor M. T., Marchler G., Marchler-Bauer A., Ruis H., Estruch F., Schüller C. 1996; The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–2235
    [Google Scholar]
20. Mollapour M., Piper P. W. 2001; Targeted gene deletion in Zygosaccharomyces bailii . Yeast 18:173–186 [CrossRef]
    [Google Scholar]
21. Panaretou B., Piper P. W. 1992; The plasma membrane of yeast acquires a novel heat-shock protein (hsp30) and displays a decline in proton-pumping ATPase levels in response to both heat shock and the entry to stationary phase. Eur J Biochem 206:635–640 [CrossRef]
    [Google Scholar]
22. Pearce A. K., Booth I. R., Brown A. J. P. 2001; Genetic manipulation of 6-phosphofructo-1-kinase and fructose 2,6-bisphosphate levels affects the extent to which benzoic acid inhibits the growth of Saccharomyces cerevisiae . Microbiology 147:403–410
    [Google Scholar]
23. Pilkington B. J., Rose A. H. 1988; Reactions of Saccharomyces cerevisiae and Zygosaccharomyces bailii to sulphite. J Gen Microbiol 134:2823–2830
    [Google Scholar]
24. 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]
25. Piper P. W., Ortiz-Calderon C., Holyoak C., Coote P., Cole M. 1997; Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevisiae , is a stress-inducible regulator of plasma membrane ATPase. Cell Stress Chaperones 2:12–24 [CrossRef]
    [Google Scholar]
26. Piper P., 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]
27. Pretorius I. S. 2000; Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729 [CrossRef]
    [Google Scholar]
28. Russell A. D. 1991; Mechanisms of bacterial resistance to non-antibiotics: food additives and food and pharmaceutical preservatives. J Appl Bacteriol 71:191–201 [CrossRef]
    [Google Scholar]
29. Salmond C. V., Kroll R. G., Booth I. R. 1984; The effects of food preservatives on pH homeostasis in Escherichia coli . J Gen Microbiol 130:2845–2850
    [Google Scholar]
30. Serrano R. 1991; Transport across yeast vacuolar and plasma membranes. In The Molecular Biology of the Yeast Saccharomyces . pp 523–586 Edited by Broach J. R., Pringle J., Jones E. W. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
31. Seymour I. J., Piper P. W. 1999; Stress induction of HSP30 , the plasma membrane heat shock protein gene of Saccharomyces cerevisiae , appears not to use known stress-regulated transcription factors. Microbiology 145:231–239 [CrossRef]
    [Google Scholar]
32. Sousa M. J., Miranda L., Cõrte-Real M., Leão C. 1996; Transport of acetic-acid in Zygosaccharomyces bailii – effects of ethanol and their implications on the resistance of the yeast to acidic environments. Appl Environ Microbiol 62:3152–3157
    [Google Scholar]
33. Sousa M. J., Rodrigues F., Cõrte-Real M., Leão C. 1998; Mechanisms underlying the transport and intracellular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii . Microbiology 144:665–670 [CrossRef]
    [Google Scholar]
34. Steels H., James S. A., Roberts I. N., Stratford M. 1999; Zygosaccharomyces lentus : a significant new osmophilic, preservative-resistant spoilage yeast, capable of growth at low temperature. J Appl Microbiol 87:520–527 [CrossRef]
    [Google Scholar]
35. Steels H., James S. A., Roberts I. N., Stratford M. 2000; Sorbic acid resistance: the inoculum effect. Yeast 16:1173–1183 [CrossRef]
    [Google Scholar]
36. Stratford M., Anslow P. A. 1996; Comparison of the inhibitory action on Saccharomyces cerevisiae of weak-acid preservatives, uncouplers, and medium-chain fatty acids. FEMS Microbiol Lett 142:53–58 [CrossRef]
    [Google Scholar]
37. 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]
38. Tenreiro S., Rosa P. C., Viegas C. A., Sa-Correia I. 2000; Expression of the AZR1 gene (ORF YGR224w), encoding a plasma membrane transporter of the major facilitator superfamily, is required for adaptation to acetic acid and resistance to azoles in Saccharomyces cerevisiae . Yeast 16:1469–1481 [CrossRef]
    [Google Scholar]
39. Thomas D. S., Davenport R. R. 1985; Zygosaccharomyces bailii – a profile of characteristics and spoilage activities. Food Microbiol 2:157–169 [CrossRef]
    [Google Scholar]
40. Verduyn C., Postma E., Scheffers W. A., Van Dijken J. P. 1992; Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501–517 [CrossRef]
    [Google Scholar]
41. 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]
42. Warth A. D. 1977; Mechanism of resistance of Saccharomyces bailii to benzoic, sorbic and other weak acids used as food preservatives. J Appl Bacteriol 43:215–230 [CrossRef]
    [Google Scholar]
43. Warth A. D. 1988; Effect of benzoic acid on growth yield of yeasts differing in their resistance to preservatives. Appl Environ Microbiol 54:2091–2095
    [Google Scholar]
44. Warth A. D. 1989; Transport of benzoic and propanoic acids by Zygosaccharomyces bailii . J Gen Microbiol 135:1383–1390
    [Google Scholar]
45. Warth A. D., Nickerson K. W. 1991; Mechanism of action of benzoic acid on Zygosaccharomyces bailii – effects on glycolytic metabolite levels, energy production, and intracellular pH. Appl Environ Microbiol 57:3410–3414
    [Google Scholar]
46. Weber F. J., de Bont J. A. M. 1996; Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim Biophys Acta 1286:225–245 [CrossRef]
    [Google Scholar]