1887

Abstract

The mechanism by which methionine relieves the growth inhibition of K-12 that is caused by organic weak acid food preservatives was investigated. In the presence of 8 mM acetate the specific growth rate of Frag1 (in MacIlvaine’s minimal medium pH 60) is reduced by 50%. Addition of methionine restores growth to 80% of that observed in untreated controls. Similar relief was seen with cultures treated with either benzoate or propionate. Mutants with an elevated intracellular methionine pool were almost completely resistant to the inhibitory effects of acetate, suggesting that the methionine pool becomes limiting for growth in acetate-treated cells. Measurement of the intracellular concentrations of pathway intermediates revealed that the homocysteine pool is increased dramatically in acetate-treated cells, suggesting that acetate inhibits a biosynthetic step downstream from this intermediate. Supplementation of the medium with homocysteine inhibits the growth of cells. Acetate inhibition of growth arises from the depletion of the intracellular methionine pool with the concomitant accumulation of the toxic intermediate homocysteine and this augments the effect of lowering cytoplasmic pH.

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2002-07-01
2019-09-21
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References

  1. Amann, E., Ochs, B. & Abel, K. J. ( 1988; ). Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69, 301-315.[CrossRef]
    [Google Scholar]
  2. Amezaga, M. R., Davidson, I., McLaggan, D., Verheul, A., Abee, T. & Booth, I. R. ( 1995; ). The role of peptide metabolism in the growth of Listeria monocytogenes ATCC 23074 at high osmolarity. Microbiology 141, 41-49.[CrossRef]
    [Google Scholar]
  3. Arnold, C. N., McElhanon, J., Lee, A., Leonhart, R. & Siegele, D. A. ( 2001; ). Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J Bacteriol 183, 2178-2186.[CrossRef]
    [Google Scholar]
  4. Bakker, E. P. & Mangerich, W. E. ( 1983; ). The effects of weak acids on potassium uptake by Escherichia coli K-12 inhibition by low cytoplasmic pH. Biochim Biophys Acta 730, 379-386.[CrossRef]
    [Google Scholar]
  5. Blankenhorn, D., Phillips, J. & Slonczewski, J. L. ( 1999; ). Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J Bacteriol 181, 2209-2216.
    [Google Scholar]
  6. Booth, I. R. ( 1985; ). Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49, 359-378.
    [Google Scholar]
  7. 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]
  8. Brul, S. & Coote, P. ( 1999; ). Preservative agents in foods. Mode of action and microbial resistance mechanisms. Int J Food Microbiol 50, 1-17.[CrossRef]
    [Google Scholar]
  9. Castanie-Cornet, M. P., Penfound, T. A., Smith, D., Elliott, J. F. & Foster, J. W. ( 1999; ). Control of acid resistance in Escherichia coli. J Bacteriol 181, 3525-3535.
    [Google Scholar]
  10. Cherrington, C. A., Hinton, M., Mead, G. C. & Chopra, I. ( 1991; ). Organic acids: chemistry, antibacterial activity and practical applications. Adv Microb Physiol 32, 87-108.
    [Google Scholar]
  11. Cole, M. B. & Keenan, M. H. ( 1986; ). Synergistic effects of weak-acid preservatives and pH on the growth of Zygosaccharomyces bailii. Yeast 2, 93-100.[CrossRef]
    [Google Scholar]
  12. Eklund, T. ( 1980; ). Inhibition of growth and uptake processes in bacteria by some chemical food preservatives. J Appl Bacteriol 48, 423-432.[CrossRef]
    [Google Scholar]
  13. Epstein, W. & Kim, B. S. ( 1971; ). Potassium transport loci in Escherichia coli. J Bacterol 108, 639-644.
    [Google Scholar]
  14. Freese, E., Sheu, C. W. & Galliers, E. ( 1973; ). Function of lipophilic acids as antimicrobial food additives. Nature 241, 321-325.[CrossRef]
    [Google Scholar]
  15. Gage, D. J. & Neidhardt, F. C. ( 1993; ). Modulation of the heat shock response by one-carbon metabolism in Escherichia coli. J Bacteriol 175, 1961-1970.
    [Google Scholar]
  16. Gonzalez, J. C., Banerjee, R. V., Huang, S., Sumner, J. S. & Matthews, R. G. ( 1992; ). Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: two solutions to the same chemical problem. Biochemistry 31, 6045-6056.[CrossRef]
    [Google Scholar]
  17. Greene, R. C. ( 1996; ). Biosynthesis of methionine. In Escherichia coli and Salmonella: Cellular and Molecular Biology , pp. 542-560. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
  18. Greene, R. C., Hunter, J. S. & Coch, E. H. ( 1973; ). Properties of metK mutants of Escherichia coli K-12. J Bacteriol 115, 57-67.
    [Google Scholar]
  19. Hahn, G. A. & Brown, J. W. ( 1967; ). Properties of a methionyl-tRNA synthetase from Sarcina lutea. Biochim Biophys Acta 146, 264-271.[CrossRef]
    [Google Scholar]
  20. Han, K., Hong, J. & Lim, H. C. ( 1993; ). Relieving effects of glycine and methionine from acetic acid inhibition in Escherichia coli fermentation. Biotechnol Bioeng 41, 316-324.[CrossRef]
    [Google Scholar]
  21. Kroll, R. G. & Booth, I. R. ( 1981; ). The role of potassium transport in the generation of a pH gradient in Escherichia coli. Biochem J 198, 691-698.
    [Google Scholar]
  22. Lambert, L. A., Abshire, K., Blankenhorn, D. & Slonczewski, J. L. ( 1997; ). Proteins induced in Escherichia coli by benzoic acid. J Bacteriol 179, 7595-7599.
    [Google Scholar]
  23. Lee, L. W., Ravel, J. M. & Shive, W. ( 1966; ). Multimetabolite control of a biosynthetic pathway by sequential metabolites. J Biol Chem 241, 5479-5480.
    [Google Scholar]
  24. Maxon, M. E., Redfield, B., Cai, X. Y., Shoeman, R., Fujita, K., Fisher, W., Stauffer, G., Weissbach, H. & Brot, N. ( 1989; ). Regulation of methionine synthesis in Escherichia coli: effect of the MetR protein on the expression of the metE and metR genes. Proc Natl Acad Sci USA 86, 85-89.[CrossRef]
    [Google Scholar]
  25. Mulvey, M. R., Switala, J., Borys, A. & Loewen, P. C. ( 1990; ). Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol 172, 6713-6720.
    [Google Scholar]
  26. Pomposiello, P. J., Bennik, M. H. & Demple, B. ( 2001; ). Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183, 3890-3902.[CrossRef]
    [Google Scholar]
  27. Roe, A. J., McLaggan, D., Davidson, I., O’Byrne, C. & Booth, I. R. ( 1998; ). Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J Bacteriol 180, 767-772.
    [Google Scholar]
  28. Ron, E. Z. & Davis, B. D. ( 1971; ). Growth rate of Escherichia coli at elevated temperatures: limitation by methionine. J Bacteriol 107, 391-396.
    [Google Scholar]
  29. Russell, J. B. & Diez-Gonzalez, F. ( 1998; ). The effects of fermentation acids on bacterial growth. Adv Microb Physiol 39, 205-234.
    [Google Scholar]
  30. Salmond, C. V., Kroll, R. G. & Booth, I. R. ( 1984; ). The effect of food preservatives on pH homeostasis in Escherichia coli. J Gen Microbiol 130, 2845-2850.
    [Google Scholar]
  31. Schellhorn, H. E. & Stones, V. L. ( 1992; ). Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol 174, 4769-4776.
    [Google Scholar]
  32. Sekowska, A., Kung, H. F. & Danchin, A. ( 2000; ). Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2, 145-177.
    [Google Scholar]
  33. Sheu, C. W., Konings, W. N. & Freese, E. ( 1972; ). Effects of acetate and other short-chain fatty acids on sugar and amino acid uptake of Bacillus subtilis. J Bacteriol 111, 525-530.
    [Google Scholar]
  34. Sheu, C. W., Salomon, D., Simmons, J. L., Sreevalsan, T. & Freese, E. ( 1975; ). Inhibitory effects of lipophilic acids and related compounds on bacteria and mammalian cells. Antimicrob Agents Chemother 7, 349-363.[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. Vallari, D. S. & Rock, C. O. ( 1987; ). Isolation and characterization of temperature-sensitive pantothenate kinase (coaA) mutants of Escherichia coli. J Bacteriol 169, 5795-5800.
    [Google Scholar]
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