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. 1995 Jul;177(14):4097–4104. doi: 10.1128/jb.177.14.4097-4104.1995

Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli.

J Lin 1, I S Lee 1, J Frey 1, J L Slonczewski 1, J W Foster 1
PMCID: PMC177142  PMID: 7608084

Abstract

Several members of the family Enterobacteriaceae were examined for differences in extreme acid survival strategies. A surprising degree of variety was found between three related genera. The minimum growth pH of Salmonella typhimurium was shown to be significantly lower (pH 4.0) than that of either Escherichia coli (pH 4.4) or Shigella flexneri (pH 4.8), yet E. coli and S. flexneri both survive exposure to lower pH levels (2 to 2.5) than S. typhimurium (pH 3.0) in complex medium. S. typhimurium and E. coli but not S. flexneri expressed low-pH-inducible log-phase and stationary-phase acid tolerance response (ATR) systems that function in minimal or complex medium to protect cells to pH 3.0. All of the organisms also expressed a pH-independent general stress resistance system that contributed to acid survival during stationary phase. E. coli and S. flexneri possessed several acid survival systems (termed acid resistance [AR]) that were not demonstrable in S. typhimurium. These additional AR systems protected cells to pH 2.5 and below but required supplementation of minimal medium for either induction or function. One acid-inducible AR system required oxidative growth in complex medium for expression but successfully protected cells to pH 2.5 in unsupplemented minimal medium, while two other AR systems important for fermentatively grown cells required the addition of either glutamate or arginine during pH 2.5 acid challenge. The arginine AR system was only observed in E. coli and required stationary-phase induction in acidified complex medium. The product of the adi locus, arginine decarboxylase, was responsible for arginine-based acid survival.

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Selected References

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  1. 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]
  2. Birkmann A., Böck A. Characterization of a cis regulatory DNA element necessary for formate induction of the formate dehydrogenase gene (fdhF) of Escherichia coli. Mol Microbiol. 1989 Feb;3(2):187–195. doi: 10.1111/j.1365-2958.1989.tb01807.x. [DOI] [PubMed] [Google Scholar]
  3. Bullas L. R., Ryu J. I. Salmonella typhimurium LT2 strains which are r- m+ for all three chromosomally located systems of DNA restriction and modification. J Bacteriol. 1983 Oct;156(1):471–474. doi: 10.1128/jb.156.1.471-474.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Casiano-Colón A., Marquis R. E. Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microbiol. 1988 Jun;54(6):1318–1324. doi: 10.1128/aem.54.6.1318-1324.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clements J. D., Flint D. C., Klipstein F. A. Immunological and physicochemical characterization of heat-labile enterotoxins isolated from two strains of Escherichia coli. Infect Immun. 1982 Nov;38(2):806–809. doi: 10.1128/iai.38.2.806-809.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fields P. I., Swanson R. V., Haidaris C. G., Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189–5193. doi: 10.1073/pnas.83.14.5189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Foster J. W., Aliabadi Z. pH-regulated gene expression in Salmonella: genetic analysis of aniG and cloning of the earA regulator. Mol Microbiol. 1989 Nov;3(11):1605–1615. doi: 10.1111/j.1365-2958.1989.tb00146.x. [DOI] [PubMed] [Google Scholar]
  8. Foster J. W., Bearson B. Acid-sensitive mutants of Salmonella typhimurium identified through a dinitrophenol lethal screening strategy. J Bacteriol. 1994 May;176(9):2596–2602. doi: 10.1128/jb.176.9.2596-2602.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Foster J. W., Hall H. K. Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron- and pH-regulated protein synthesis. J Bacteriol. 1992 Jul;174(13):4317–4323. doi: 10.1128/jb.174.13.4317-4323.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Foster J. W., Park Y. K., Bang I. S., Karem K., Betts H., Hall H. K., Shaw E. Regulatory circuits involved with pH-regulated gene expression in Salmonella typhimurium. Microbiology. 1994 Feb;140(Pt 2):341–352. doi: 10.1099/13500872-140-2-341. [DOI] [PubMed] [Google Scholar]
  13. Foster J. W. Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol. 1991 Nov;173(21):6896–6902. doi: 10.1128/jb.173.21.6896-6902.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Foster J. W. The acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. J Bacteriol. 1993 Apr;175(7):1981–1987. doi: 10.1128/jb.175.7.1981-1987.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gorden J., Small P. L. Acid resistance in enteric bacteria. Infect Immun. 1993 Jan;61(1):364–367. doi: 10.1128/iai.61.1.364-367.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell. 1993 Jan 29;72(2):165–168. doi: 10.1016/0092-8674(93)90655-a. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Hoiseth S. K., Stocker B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 1981 May 21;291(5812):238–239. doi: 10.1038/291238a0. [DOI] [PubMed] [Google Scholar]
  19. Lee I. S., Slonczewski J. L., Foster J. W. A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. J Bacteriol. 1994 Mar;176(5):1422–1426. doi: 10.1128/jb.176.5.1422-1426.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MELNYKOVYCH G., SNELL E. E. Nutritional requirements for the formation of arginine decarboxylase in Escherichia coli. J Bacteriol. 1958 Nov;76(5):518–523. doi: 10.1128/jb.76.5.518-523.1958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maloy S. R., Roth J. R. Regulation of proline utilization in Salmonella typhimurium: characterization of put::Mu d(Ap, lac) operon fusions. J Bacteriol. 1983 May;154(2):561–568. doi: 10.1128/jb.154.2.561-568.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Meng S. Y., Bennett G. N. Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol. 1992 Apr;174(8):2659–2669. doi: 10.1128/jb.174.8.2659-2669.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Neely M. N., Dell C. L., Olson E. R. Roles of LysP and CadC in mediating the lysine requirement for acid induction of the Escherichia coli cad operon. J Bacteriol. 1994 Jun;176(11):3278–3285. doi: 10.1128/jb.176.11.3278-3285.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Hara G. W., Glenn A. R. The adaptive acid tolerance response in root nodule bacteria and Escherichia coli. Arch Microbiol. 1994;161(4):286–292. doi: 10.1007/BF00303582. [DOI] [PubMed] [Google Scholar]
  25. Raja N., Goodson M., Chui W. C., Smith D. G., Rowbury R. J. Habituation to acid in Escherichia coli: conditions for habituation and its effects on plasmid transfer. J Appl Bacteriol. 1991 Jan;70(1):59–65. doi: 10.1111/j.1365-2672.1991.tb03787.x. [DOI] [PubMed] [Google Scholar]
  26. Rowbury R. J., Goodson M., Wallace A. D. The PhoE porin and transmission of the chemical stimulus for induction of acid resistance (acid habituation) in Escherichia coli. J Appl Bacteriol. 1992 Mar;72(3):233–243. doi: 10.1111/j.1365-2672.1992.tb01829.x. [DOI] [PubMed] [Google Scholar]
  27. Schlensog V., Böck A. Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system of Escherichia coli. Mol Microbiol. 1990 Aug;4(8):1319–1327. doi: 10.1111/j.1365-2958.1990.tb00711.x. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Small P., Blankenhorn D., Welty D., Zinser E., Slonczewski J. L. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol. 1994 Mar;176(6):1729–1737. doi: 10.1128/jb.176.6.1729-1737.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stim K. P., Bennett G. N. Nucleotide sequence of the adi gene, which encodes the biodegradative acid-induced arginine decarboxylase of Escherichia coli. J Bacteriol. 1993 Mar;175(5):1221–1234. doi: 10.1128/jb.175.5.1221-1234.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]

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