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

C. D. Holyoak, M. Stratford, Z. Mcmullin, M. B. Cole, K. Crimmins, A. J.P. Brown, P. J. Coote*

*Corresponding author for this work

Research output: Contribution to journalArticle

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Abstract

The weak acid sorbic acid transiently inhibited the growth of Saccharomyces cerevisiae in media at low pH. During a lag period, the length of which depended on the severity of this weak-acid stress, yeast cells appeared to adapt to this stress, eventually recovering and growing normally. This adaptation to weak-acid stress was not due to metabolism and removal of the sorbic acid. A pma1-205 mutant, with about half the normal membrane H+- ATPase activity, was shown to be more sensitive to sorbic acid than its parent. Sorbic acid appeared to stimulate plasma membrane H+-ATPase activity in both PMA1 and pma1-205. Consistent with this, cellular ATP levels showed drastic reductions, the extent of which depended on the severity of weak- acid stress. The weak acid did not appear to affect the synthesis of ATP because CO2 production and O2 consumption were not affected significantly in PMA1 and pma1-205 cells. However, a glycolytic mutant, with about one- third the normal pyruvate kinase and phosphofructokinase activity and hence a reduced capacity to generate ATP, was more sensitive to sorbic acid than its isogenic parent. These data are consistent with the idea that adaptation by yeast cells to sorbic acid is dependent on (i) the restoration of internal pH via the export of protons by the membrane H+-ATPase in an energy-demanding process and (ii) the generation of sufficient ATP to drive this process and still allow growth.

Original languageEnglish
Pages (from-to)3158-3164
Number of pages7
JournalAPPLIED AND ENVIRONMENTAL MICROBIOLOGY
Volume62
Issue number9
Publication statusPublished - 1 Sep 1996

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Sorbic Acid
sorbic acid
H-transporting ATP synthase
Proton-Translocating ATPases
preservative
preservatives
Saccharomyces cerevisiae
plasma membrane
Cell Membrane
membrane
plasma
Acids
acids
acid
Growth
Adenosine Triphosphate
Yeasts
yeasts
process energy
Phosphofructokinases

ASJC Scopus subject areas

  • Biotechnology
  • Food Science
  • Applied Microbiology and Biotechnology
  • Ecology

Cite this

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. / Holyoak, C. D.; Stratford, M.; Mcmullin, Z.; Cole, M. B.; Crimmins, K.; Brown, A. J.P.; Coote, P. J.

In: APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Vol. 62, No. 9, 01.09.1996, p. 3158-3164.

Research output: Contribution to journalArticle

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abstract = "The weak acid sorbic acid transiently inhibited the growth of Saccharomyces cerevisiae in media at low pH. During a lag period, the length of which depended on the severity of this weak-acid stress, yeast cells appeared to adapt to this stress, eventually recovering and growing normally. This adaptation to weak-acid stress was not due to metabolism and removal of the sorbic acid. A pma1-205 mutant, with about half the normal membrane H+- ATPase activity, was shown to be more sensitive to sorbic acid than its parent. Sorbic acid appeared to stimulate plasma membrane H+-ATPase activity in both PMA1 and pma1-205. Consistent with this, cellular ATP levels showed drastic reductions, the extent of which depended on the severity of weak- acid stress. The weak acid did not appear to affect the synthesis of ATP because CO2 production and O2 consumption were not affected significantly in PMA1 and pma1-205 cells. However, a glycolytic mutant, with about one- third the normal pyruvate kinase and phosphofructokinase activity and hence a reduced capacity to generate ATP, was more sensitive to sorbic acid than its isogenic parent. These data are consistent with the idea that adaptation by yeast cells to sorbic acid is dependent on (i) the restoration of internal pH via the export of protons by the membrane H+-ATPase in an energy-demanding process and (ii) the generation of sufficient ATP to drive this process and still allow growth.",
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note = "We thank R. Serrano for providing strains; G. Collins, Analytical Department, Unilever Research, for HPLC determination of sorbic acid concentrations; and I. Booth for discussion regarding pHi homeostasis and for suggesting the experiments involving the glycolytic mutants. Many thanks are also due to P. W. Piper for helpful discussion and C. P. O’Byrne for critical reading of the manuscript.",
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AU - Stratford, M.

AU - Mcmullin, Z.

AU - Cole, M. B.

AU - Crimmins, K.

AU - Brown, A. J.P.

AU - Coote, P. J.

N1 - We thank R. Serrano for providing strains; G. Collins, Analytical Department, Unilever Research, for HPLC determination of sorbic acid concentrations; and I. Booth for discussion regarding pHi homeostasis and for suggesting the experiments involving the glycolytic mutants. Many thanks are also due to P. W. Piper for helpful discussion and C. P. O’Byrne for critical reading of the manuscript.

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N2 - The weak acid sorbic acid transiently inhibited the growth of Saccharomyces cerevisiae in media at low pH. During a lag period, the length of which depended on the severity of this weak-acid stress, yeast cells appeared to adapt to this stress, eventually recovering and growing normally. This adaptation to weak-acid stress was not due to metabolism and removal of the sorbic acid. A pma1-205 mutant, with about half the normal membrane H+- ATPase activity, was shown to be more sensitive to sorbic acid than its parent. Sorbic acid appeared to stimulate plasma membrane H+-ATPase activity in both PMA1 and pma1-205. Consistent with this, cellular ATP levels showed drastic reductions, the extent of which depended on the severity of weak- acid stress. The weak acid did not appear to affect the synthesis of ATP because CO2 production and O2 consumption were not affected significantly in PMA1 and pma1-205 cells. However, a glycolytic mutant, with about one- third the normal pyruvate kinase and phosphofructokinase activity and hence a reduced capacity to generate ATP, was more sensitive to sorbic acid than its isogenic parent. These data are consistent with the idea that adaptation by yeast cells to sorbic acid is dependent on (i) the restoration of internal pH via the export of protons by the membrane H+-ATPase in an energy-demanding process and (ii) the generation of sufficient ATP to drive this process and still allow growth.

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