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. 1985 Dec;164(3):1224–1232. doi: 10.1128/jb.164.3.1224-1232.1985

Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system.

J Cairney, I R Booth, C F Higgins
PMCID: PMC219319  PMID: 3905768

Abstract

Previous evidence has indicated that a gene, proU, is involved in the response of bacterial cells to growth at high osmolarity. Using Mu-mediated lacZ operon fusions we found that transcription of the proU gene of Salmonella typhimurium is stimulated over 100-fold in response to increases in external osmolarity. Our evidence suggests that changes in turgor pressure are responsible for these alterations in gene expression. Expression of proU is independent of the ompR gene, known to be involved in osmoregulation of porin expression. Thus, there must be at least two distinct mechanisms by which external osmolarity can influence gene expression. We show that there are relatively few genes in the cell which are under such osmotic control. The proU gene is shown to encode a high-affinity transport system (Km = 1.3 microM) for the osmoprotectant betaine, which is accumulated to high concentrations in response to osmotic stress. Even when fully induced, this transport system is only able to function in medium of high osmolarity. Thus, betaine transport is regulated by osmotic pressure at two levels: the induction of expression and by modulation of activity of the transport proteins. We have previously shown that the proP gene encodes a lower-affinity betaine transport system (J. Cairney, I. R. Booth, and C. F. Higgins, J. Bacteriol., 164:1218-1223, 1985). In proP proU strains, no saturable betaine uptake could be detected although there was a low-level nonsaturable component at high substrate concentrations. Thus, S. typhimurium has two genetically distinct pathways for betaine uptake, a constitutive low-affinity system (proP) and an osmotically induced high-affinity system (proU).

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Selected References

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  1. Alphen W. V., Lugtenberg B. Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol. 1977 Aug;131(2):623–630. doi: 10.1128/jb.131.2.623-630.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cairney J., Booth I. R., Higgins C. F. Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol. 1985 Dec;164(3):1218–1223. doi: 10.1128/jb.164.3.1218-1223.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. Csonka L. N., Howe M. M., Ingraham J. L., Pierson L. S., 3rd, Turnbough C. L., Jr Infection of Salmonella typhimurium with coliphage Mu d1 (Apr lac): construction of pyr::lac gene fusions. J Bacteriol. 1981 Jan;145(1):299–305. doi: 10.1128/jb.145.1.299-305.1981. [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. Dunlap V. J., Csonka L. N. Osmotic regulation of L-proline transport in Salmonella typhimurium. J Bacteriol. 1985 Jul;163(1):296–304. doi: 10.1128/jb.163.1.296-304.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gibson M. M., Price M., Higgins C. F. Genetic characterization and molecular cloning of the tripeptide permease (tpp) genes of Salmonella typhimurium. J Bacteriol. 1984 Oct;160(1):122–130. doi: 10.1128/jb.160.1.122-130.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hall M. N., Silhavy T. J. Genetic analysis of the major outer membrane proteins of Escherichia coli. Annu Rev Genet. 1981;15:91–142. doi: 10.1146/annurev.ge.15.120181.000515. [DOI] [PubMed] [Google Scholar]
  11. Hall M. N., Silhavy T. J. Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol. 1981 Sep 5;151(1):1–15. doi: 10.1016/0022-2836(81)90218-7. [DOI] [PubMed] [Google Scholar]
  12. Hall M. N., Silhavy T. J. The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K12. J Mol Biol. 1981 Feb 15;146(1):23–43. doi: 10.1016/0022-2836(81)90364-8. [DOI] [PubMed] [Google Scholar]
  13. Hughes K. T., Roth J. R. Conditionally transposition-defective derivative of Mu d1(Amp Lac). J Bacteriol. 1984 Jul;159(1):130–137. doi: 10.1128/jb.159.1.130-137.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Kennedy E. P. Osmotic regulation and the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1092–1095. doi: 10.1073/pnas.79.4.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kleckner N., Chan R. K., Tye B. K., Botstein D. Mutagenesis by insertion of a drug-resistance element carrying an inverted repetition. J Mol Biol. 1975 Oct 5;97(4):561–575. doi: 10.1016/s0022-2836(75)80059-3. [DOI] [PubMed] [Google Scholar]
  17. Laimins L. A., Rhoads D. B., Epstein W. Osmotic control of kdp operon expression in Escherichia coli. Proc Natl Acad Sci U S A. 1981 Jan;78(1):464–468. doi: 10.1073/pnas.78.1.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. 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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