Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Nov;173(21):6896–6902. doi: 10.1128/jb.173.21.6896-6902.1991

Salmonella acid shock proteins are required for the adaptive acid tolerance response.

J W Foster 1
PMCID: PMC209043  PMID: 1938893

Abstract

Salmonella typhimurium, as well as other enteric bacteria, experiences significant fluctuations in H+ ion concentrations during growth in diverse ecological niches. In fact, some pH conditions which should kill cells rapidly, such as stomach acidity, are nevertheless tolerated. The complete mechanism for this tolerance is unknown. However, I have recently demonstrated that S. typhimurium has the ability to survive extreme low pH (pH 3.0 to 4.0) if first adapted to mild pH (pH 5.5 to 6.0). This phenomenon has been referred to as the acidification tolerance response (ATR). The exposure to mild acid is referred to as preshock, and the proteins involved are called preshock ATR proteins. A second type of encounter with acid, called acid shock, involves shifting cells directly from alkaline conditions (pH 7.7) to acid conditions (pH 4.5 or below). During acid shock, the organism immediately ceases reproduction and dramatically changes the expression of at least 52 proteins. All but four are distinct from the preshock ATR proteins. Surprisingly, acid shock alone did not afford significant protection against strong acid challenge in minimal medium. Furthermore, inhibiting protein synthesis prior to acid shock revealed that the acid shock proteins do not appear to contribute to acid survival in minimal medium even at pH 4.3. Constitutive cellular pH homeostatic mechanisms seem sufficient to protect cells at this pH. The data suggest that the induction of acid shock and preshock ATR proteins are separate processes requiring separate signals. However, for S. typhimurium to survive extreme acid conditions, it must induce both the preshock and acid shock systems. Preventing the expression of one or the other eliminates acid tolerance. I propose a two-stage process that allows S. typhimurium to phase in acid tolerance as the environmental pH becomes progressively more acidic.

Full text

PDF
6896

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aliabadi Z., Park Y. K., Slonczewski J. L., Foster J. W. Novel regulatory loci controlling oxygen- and pH-regulated gene expression in Salmonella typhimurium. J Bacteriol. 1988 Feb;170(2):842–851. doi: 10.1128/jb.170.2.842-851.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auger E. A., Redding K. E., Plumb T., Childs L. C., Meng S. Y., Bennett G. N. Construction of lac fusions to the inducible arginine- and lysine decarboxylase genes of Escherichia coli K12. Mol Microbiol. 1989 May;3(5):609–620. doi: 10.1111/j.1365-2958.1989.tb00208.x. [DOI] [PubMed] [Google Scholar]
  3. Booth I. R. Regulation of cytoplasmic pH in bacteria. Microbiol Rev. 1985 Dec;49(4):359–378. doi: 10.1128/mr.49.4.359-378.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buchmeier N. A., Heffron F. Induction of Salmonella stress proteins upon infection of macrophages. Science. 1990 May 11;248(4956):730–732. doi: 10.1126/science.1970672. [DOI] [PubMed] [Google Scholar]
  5. Finlay B. B., Falkow S. Salmonella as an intracellular parasite. Mol Microbiol. 1989 Dec;3(12):1833–1841. doi: 10.1111/j.1365-2958.1989.tb00170.x. [DOI] [PubMed] [Google Scholar]
  6. Foster J. W., Hall H. K. Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol. 1990 Feb;172(2):771–778. doi: 10.1128/jb.172.2.771-778.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Foster J. W., Hall H. K. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol. 1991 Aug;173(16):5129–5135. doi: 10.1128/jb.173.16.5129-5135.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gale E. F., Epps H. M. The effect of the pH of the medium during growth on the enzymic activities of bacteria (Escherichia coli and Micrococcus lysodeikticus) and the biological significance of the changes produced. Biochem J. 1942 Sep;36(7-9):600–618. doi: 10.1042/bj0360600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Heyde M., Portalier R. Acid shock proteins of Escherichia coli. FEMS Microbiol Lett. 1990 May;57(1-2):19–26. doi: 10.1016/0378-1097(90)90406-g. [DOI] [PubMed] [Google Scholar]
  10. Hickey E. W., Hirshfield I. N. Low-pH-induced effects on patterns of protein synthesis and on internal pH in Escherichia coli and Salmonella typhimurium. Appl Environ Microbiol. 1990 Apr;56(4):1038–1045. doi: 10.1128/aem.56.4.1038-1045.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Macnab R. M., Castle A. M. A variable stoichiometry model for pH homeostasis in bacteria. Biophys J. 1987 Oct;52(4):637–647. doi: 10.1016/S0006-3495(87)83255-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Minton K. W., Karmin P., Hahn G. M., Minton A. P. Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: a model for the biological role of heat shock proteins. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7107–7111. doi: 10.1073/pnas.79.23.7107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ohkuma S., Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3327–3331. doi: 10.1073/pnas.75.7.3327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Padan E., Schuldiner S. Intracellular pH and membrane potential as regulators in the prokaryotic cell. J Membr Biol. 1987;95(3):189–198. doi: 10.1007/BF01869481. [DOI] [PubMed] [Google Scholar]
  15. Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
  16. Skowyra D., Georgopoulos C., Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990 Sep 7;62(5):939–944. doi: 10.1016/0092-8674(90)90268-j. [DOI] [PubMed] [Google Scholar]
  17. Slonczewski J. L., Gonzalez T. N., Bartholomew F. M., Holt N. J. Mu d-directed lacZ fusions regulated by low pH in Escherichia coli. J Bacteriol. 1987 Jul;169(7):3001–3006. doi: 10.1128/jb.169.7.3001-3006.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Spector M. P., Aliabadi Z., Gonzalez T., Foster J. W. Global control in Salmonella typhimurium: two-dimensional electrophoretic analysis of starvation-, anaerobiosis-, and heat shock-inducible proteins. J Bacteriol. 1986 Oct;168(1):420–424. doi: 10.1128/jb.168.1.420-424.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES