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. 1985 Dec;164(3):1218–1223. doi: 10.1128/jb.164.3.1218-1223.1985

Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine.

J Cairney, I R Booth, C F Higgins
PMCID: PMC219318  PMID: 3905767

Abstract

Betaine (N,N,N-trimethylglycine) can be accumulated to high intracellular concentrations and serves an important osmoprotective function in enteric bacteria. We found that the proP gene of Salmonella typhimurium, originally identified as encoding a minor transport system for proline (permease PP-II), plays an important role in betaine uptake. Mutations in proP reduced the ability of betaine to serve as an osmoprotectant. Transport of betaine into the cells was also severely impaired in these mutants. The kinetics of uptake via PP-II suggest that betaine, rather than proline, is the important physiological substrate for this transport system. Betaine uptake via PP-II was regulated by osmotic pressure at two different levels: transcription of the proP gene was increased by increasing osmolarity, and, in addition, activity of the transport system itself was dependent upon the osmotic pressure of the medium. The specificity of the transport system was also altered by increasing osmolarity which enhanced the affinity for betaine while reducing that for proline.

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Selected References

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

  1. Anderson R. R., Menzel R., Wood J. M. Biochemistry and regulation of a second L-proline transport system in Salmonella typhimurium. J Bacteriol. 1980 Mar;141(3):1071–1076. doi: 10.1128/jb.141.3.1071-1076.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N. Positive selection for loss of tetracycline resistance. J Bacteriol. 1980 Aug;143(2):926–933. doi: 10.1128/jb.143.2.926-933.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cairney J., Booth I. R., Higgins C. F. Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. J Bacteriol. 1985 Dec;164(3):1224–1232. doi: 10.1128/jb.164.3.1224-1232.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cairney J., Higgins C. F., Booth I. R. Proline uptake through the major transport system of Salmonella typhimurium is coupled to sodium ions. J Bacteriol. 1984 Oct;160(1):22–27. doi: 10.1128/jb.160.1.22-27.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Csonka L. N. A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength. J Bacteriol. 1982 Sep;151(3):1433–1443. doi: 10.1128/jb.151.3.1433-1443.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Csonka L. N. Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet. 1981;182(1):82–86. doi: 10.1007/BF00422771. [DOI] [PubMed] [Google Scholar]
  8. Gould G. W., Measures J. C. Water relations in single cells. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 29;278(959):151–166. doi: 10.1098/rstb.1977.0035. [DOI] [PubMed] [Google Scholar]
  9. Harshman R. B., Yamazaki H. MSI accumulation induced by sodium chloride. Biochemistry. 1972 Feb 15;11(4):615–618. doi: 10.1021/bi00754a023. [DOI] [PubMed] [Google Scholar]
  10. Imhoff J. F., Rodriguez-Valera F. Betaine is the main compatible solute of halophilic eubacteria. J Bacteriol. 1984 Oct;160(1):478–479. doi: 10.1128/jb.160.1.478-479.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Le Rudulier D., Bouillard L. Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae. Appl Environ Microbiol. 1983 Jul;46(1):152–159. doi: 10.1128/aem.46.1.152-159.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Le Rudulier D., Strom A. R., Dandekar A. M., Smith L. T., Valentine R. C. Molecular biology of osmoregulation. Science. 1984 Jun 8;224(4653):1064–1068. doi: 10.1126/science.224.4653.1064. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Menzel R., Roth J. Identification and mapping of a second proline permease Salmonella typhimurium. J Bacteriol. 1980 Mar;141(3):1064–1070. doi: 10.1128/jb.141.3.1064-1070.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Perroud B., Le Rudulier D. Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol. 1985 Jan;161(1):393–401. doi: 10.1128/jb.161.1.393-401.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ratzkin B., Grabnar M., Roth J. Regulation of the major proline permease gene of Salmonella typhimurium. J Bacteriol. 1978 Feb;133(2):737–743. doi: 10.1128/jb.133.2.737-743.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ratzkin B., Roth J. Cluster of genes controlling proline degradation in Salmonella typhimurium. J Bacteriol. 1978 Feb;133(2):744–754. doi: 10.1128/jb.133.2.744-754.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rhoads D. B., Epstein W. Cation transport in Escherichia coli. IX. Regulation of K transport. J Gen Physiol. 1978 Sep;72(3):283–295. doi: 10.1085/jgp.72.3.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Roth W. G., Leckie M. P., Dietzler D. N. Osmotic stress drastically inhibits active transport of carbohydrates by Escherichia coli. Biochem Biophys Res Commun. 1985 Jan 16;126(1):434–441. doi: 10.1016/0006-291x(85)90624-2. [DOI] [PubMed] [Google Scholar]
  20. Stalmach M. E., Grothe S., Wood J. M. Two proline porters in Escherichia coli K-12. J Bacteriol. 1983 Nov;156(2):481–486. doi: 10.1128/jb.156.2.481-486.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N. Living with water stress: evolution of osmolyte systems. Science. 1982 Sep 24;217(4566):1214–1222. doi: 10.1126/science.7112124. [DOI] [PubMed] [Google Scholar]

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