1887

Abstract

Inhibition of microbial growth by weak acid preservatives increases with medium acidification, since these agents enter cells in the undissociated state. Many of the effects of these acids are due to the cytoplasmic acidification they cause as they dissociate in the higher pH environment of the cytosol. Sorbic and benzoic acids, two widely used preservatives, were found to exert pronounced effects on the heat shock response and thermotolerance of These effects were strongly influenced by the pH of the culture medium. In low pH cultures sorbate inhibited the induction of thermotolerance by sublethal heat shock, causing strong induction of respiratory-deficient petites among the survivors of heat treatment. However, when the culture pH was above 5·5 sorbate acted as a powerful chemical inducer of thermotolerance in the absence of any sublethal heat treatment. Sorbate and benzoate also inhibited heat induction of the major heat shock proteins in low pH yeast cultures. This appears to result from lack of induction of the heat shock element (HSE) promoter sequence since sorbate prevented heat induction of a HSE- fusion at low pH. The uncoupler carbonyl cyanide -chlorophenylhydrazone (CCCP) and the plasma-membrane-ATPase inhibitor diethylstilboestrol were identified as additional inhibitors of heat induction of heat shock proteins. Numerous chemicals induce the heat shock response in the absence of heat stress, but sorbate, benzoate, CCCP and diethylstilboestrol are the first compounds shown to act as selective inhibitors of heat-induced protein expression in yeast. In the presence of sorbate concentrations which, at low pH, totally inhibit both the heat shock response and growth of cells competent in respiration, respiratory-deficient petites still retain a limited capacity for growth and for heat induction of heat shock proteins. This restoration of a response to heat shock in acidified sorbate-treated cultures of petites might contribute to their higher capacity for growth in the presence of sorbate.

Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-140-5-1085
1994-05-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/140/5/mic-140-5-1085.html?itemId=/content/journal/micro/10.1099/13500872-140-5-1085&mimeType=html&fmt=ahah

References

  1. Ananthan J., Goldberg A.L., Voellmy R.> Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 1985; 232:522–524
    [Google Scholar]
  2. Borst-Pauwels G.W.G.H.> Ion transport in yeast. Biochim Biophys Acta 1981; 650:88–127
    [Google Scholar]
  3. Cole M.B.> The effect of weak acids and pH on Zygosaccharomyces bailii 1987 PhD thesis University of East Anglia;
    [Google Scholar]
  4. Cole M.B., Keenan M.J.H.> Synergistic effects of weak acid preservatives and pH on the growth of Zjgosaccharomyces bailii. Yeast 1986; 2:93–100
    [Google Scholar]
  5. Cole M.B., Keenan M.J.H.> Effects of weak acids and external pH on the intracellular pH of Zygosaccharomyces bailii, and its implications in weak-acid resistance. Yeast 1987; 3:23–32
    [Google Scholar]
  6. Coote P.J.> Mechanisms of induced thermotolerance in Saccharomyces cerevisiae 1993 PhD thesis University of Nottingham;
    [Google Scholar]
  7. Coote P.J., Cole M.B., Jones M.V.> Induction of increased thermotolerance in Saccharomyces cerevisiae may be triggered by a mechanism involving intracellular pH. J Gen Microbiol 1991; 137:1701–1708
    [Google Scholar]
  8. Evans I.H., Wilkie D.> Mitochondrial factors in the utilisation of sugars in Saccharomyces cerevisiae. Genet Res 1976; 27:89–93
    [Google Scholar]
  9. Francois J., Van Schaftingen E., Hers H.-G.> Effect of benzoate on the metabolism of fructose 2,6-bisphosphate in yeast. Eur J Biochem 1986; 154:141–145
    [Google Scholar]
  10. Francois J., Van Schaftingen E., Hers H.-G.> Characterisation of phosphofructokinase 2 and of enzymes involved in the degradation of fructose 2,6-bisphosphate in yeast. Eur J Biochem 1988a; 171:599–608
    [Google Scholar]
  11. Francois J., Villanueva M.E., Hers H.-G.> The control of glycogen metabolism in yeast: interconversion in vivo of glycogen synthase and glycogen phosphorylase induced by glucose, a nitrogen source or uncouplers. Eur J Biochem 1988b; 174:551–559
    [Google Scholar]
  12. Hosokawa N., Hirayoshi K., Nakai A., Hosokawa Y., Marui N., Yoshida M., Sakai T., Nishino H., Aoike A., Kawai K., Nagata K.> Flavonoids inhibit the expression of heat shock proteins. Cell Struct Eunct 1990; 15:393–401
    [Google Scholar]
  13. Kirk N., Piper P.W.> The determinants of heat shock element-directed lacZ expression in Saccharomyces cerevisiae. Yeast 1991; 7:539–546
    [Google Scholar]
  14. Krebs H.A., Wiggins D., Stubbs M., Sols A., Bedoya F.> Studies on the mechanism of the antifungal action of benzoate. Biochem J 1983; 214:657–663
    [Google Scholar]
  15. Lagunas R.> Misconceptions about the energy metabolism of Saccharomyces cerevisiae. Yeast 1986; 2:221–228
    [Google Scholar]
  16. Lindquist S., Craig E.A.> The heat shock proteins. Annu Rev Crenet 1988; 55:1151–1191
    [Google Scholar]
  17. Mager W.H., Moradas-Ferreira P.> Stress response of yeast. Biochem J 1993; 290:1–13
    [Google Scholar]
  18. Mahler H.R., Wilkie D.> Mitochondrial control of sugar utilisation in Saccharomyces cerevisiae. Plasmid 1978; 1:125–133
    [Google Scholar]
  19. Marchler G., Schuller C., Adam G., Ruis H.> A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 1993; 12:1997–2003
    [Google Scholar]
  20. Miller J.H.> Experiments in Molecular Genetics 1972 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  21. Panaretou B., Piper P.W.> Plasma membrane ATPase action affects several stress tolerances of Saccharomyces cerevisiae and Schizosaccharomyces pombe as well as the extent and duration of the heat shock response. J Gen Microbiol 1990; 136:1763–1770
    [Google Scholar]
  22. Panaretou B., Piper P.W.> 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 1992; 206:635–640
    [Google Scholar]
  23. Piper P.W.> Molecular events associated with the acquisition of heat tolerance in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 1993; 11:339–356
    [Google Scholar]
  24. Russell A.D.> Mechanisms of bacterial resistance to nonantibiotics : food additives and food and pharmaceutical preservatives. J Appl Bacteriol 1991; 71:191–201
    [Google Scholar]
  25. Serrano R.> Transport across yeast vacuolar and plasma membranes. In The Molecular Biology of the Yeast Saccharomyces. Genome Dynamics, Protein Synthesis, and Energetics 1991 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; Edited by Strathern J.N., Jones E.W., Broach J.R. pp 523–585
    [Google Scholar]
  26. Sorger P.K.> Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 1990; 62:793–805
    [Google Scholar]
  27. Sorger P.K.> Heat shock factor and the heat shock response. Cell 1991; 65:363–366
    [Google Scholar]
  28. Sorger P.K., Pelham H.R.B.> Purification and characterisation of a heat-shock element binding protein from yeast. EMBO J 1987; 6:035–3041
    [Google Scholar]
  29. Sherman F., Fink G.R., Hicks J.B.> Synthetic complete medium. In Methods in Yeast Genetics 1983 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; pp 62–84
    [Google Scholar]
  30. Thevelein J.M., Beuliens M., Honshoven F., Hoebeeck G., Detremerie K., den Hollander J.A., Jans A.W.H.> Regulation of the cAMP level in the yeast Saccharomyces cerevisiae: intracellular pH and the effect of membrane depolarizing compounds. J Gen Microbiol 1987; 133:2191–2196
    [Google Scholar]
  31. Thomas D.S., Davenport R.> Zygosaccharomyces bailii-a profile of characteristics and spoilage activities. Food Microbiol 1985; 2:157–169
    [Google Scholar]
  32. Ulazewski S., Van Herckm J.-C., Dufour J.-P., Kulpa J., Nieuwenhuis B., Goffeau A.> A single mutation confers vanadate resistance to the plasma membrane H+-ATPase from the yeast Schfosaccharomyces pombe. J Biol Chem 1987; 262:223–228
    [Google Scholar]
  33. Van Uden N.> Temperature profiles of yeasts. Adv Microb Physiol 1984; 25:195–251
    [Google Scholar]
  34. Warth A.D.> Mechanism of resistance of Saccharomyces bailii to benzoic, sorbic and other weak acids used as food preservatives. J Appl Bacteriol 1978; 43:215–230
    [Google Scholar]
  35. Warth A.D.> Effects of benzoic acid on growth yields of yeasts differing in their resistance to preservatives. Appl Environ Microbiol 1988; 54:2091–2095
    [Google Scholar]
  36. Watson K.> Microbial stress proteins. Adv Microb 1990; Physiol31:183–223
    [Google Scholar]
/content/journal/micro/10.1099/13500872-140-5-1085
Loading
/content/journal/micro/10.1099/13500872-140-5-1085
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