Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1986 Aug;167(2):433–438. doi: 10.1128/jb.167.2.433-438.1986

Regulation of envelope protein composition during adaptation to osmotic stress in Escherichia coli.

A Barron, G May, E Bremer, M Villarejo
PMCID: PMC212906  PMID: 3015869

Abstract

Adaptation to osmotic stress alters the amounts of several specific proteins in the Escherichia coli K-12 envelope. The most striking feature of the response to elevated osmolarity was the strong induction of a periplasmic protein with an Mr of 31,000. This protein was absent in mutants with lambda plac Mu insertions in an osmotically inducible locus mapping near 58 min. The insertions are likely to be in proU, a locus encoding a transport activity for the osmoprotectants glycine betaine and proline. Factors affecting the extent of proU induction were identified by direct examination of periplasmic proteins on sodium dodecyl sulfate gels and by measuring beta-galactosidase activity from proU-lac fusions. Expression was stimulated by increasing additions of salt or sucrose to minimal medium, up to a maximum at 0.5 M NaCl. Exogenous glycine betaine acted as an osmoregulatory signal; its addition to the high-osmolarity medium substantially repressed the expression of the 31,000-dalton periplasmic protein and the proU-lac+ fusions. Elevated osmolarity also caused the appearance of a second periplasmic protein (Mr = 16,000), and severe reduction in the amounts of two others. In the outer membrane, the well-characterized repression of OmpF by high osmolarity was observed and was reversed by glycine betaine. Additional changes in membrane composition were also responsive to glycine betaine regulation.

Full text

PDF
438

Images in this article

434Image
on p.434
435Image
on p.435
436Image
on p.436

Selected References

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

  1. Bremer E., Silhavy T. J., Weisemann J. M., Weinstock G. M. Lambda placMu: a transposable derivative of bacteriophage lambda for creating lacZ protein fusions in a single step. J Bacteriol. 1984 Jun;158(3):1084–1093. doi: 10.1128/jb.158.3.1084-1093.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Casadaban M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. doi: 10.1016/0022-2836(76)90119-4. [DOI] [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. 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]
  7. 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]
  8. Gowrishankar J. Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J Bacteriol. 1985 Oct;164(1):434–445. doi: 10.1128/jb.164.1.434-445.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Kawaji H., Mizuno T., Mizushima S. Influence of molecular size and osmolarity of sugars and dextrans on the synthesis of outer membrane proteins O-8 and O-9 of Escherichia coli K-12. J Bacteriol. 1979 Dec;140(3):843–847. doi: 10.1128/jb.140.3.843-847.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. 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]
  15. Lugtenberg B., Peters R., Bernheimer H., Berendsen W. Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet. 1976 Sep 23;147(3):251–262. doi: 10.1007/BF00582876. [DOI] [PubMed] [Google Scholar]
  16. Measures J. C. Role of amino acids in osmoregulation of non-halophilic bacteria. Nature. 1975 Oct 2;257(5525):398–400. doi: 10.1038/257398a0. [DOI] [PubMed] [Google Scholar]
  17. Meury J., Robin A., Monnier-Champeix P. Turgor-controlled K+ fluxes and their pathways in Escherichia coli. Eur J Biochem. 1985 Sep 16;151(3):613–619. doi: 10.1111/j.1432-1033.1985.tb09148.x. [DOI] [PubMed] [Google Scholar]
  18. Munro G. F., Bell C. A., Lederman M. Multiple transport components for putrescine in Escherichia coli. J Bacteriol. 1974 Jun;118(3):952–963. doi: 10.1128/jb.118.3.952-963.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nossal N. G., Heppel L. A. The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J Biol Chem. 1966 Jul 10;241(13):3055–3062. [PubMed] [Google Scholar]
  20. 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]
  21. Pugsley A. P., Schnaitman C. A. Identification of three genes controlling production of new outer membrane pore proteins in Escherichia coli K-12. J Bacteriol. 1978 Sep;135(3):1118–1129. doi: 10.1128/jb.135.3.1118-1129.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rhoads D. B., Waters F. B., Epstein W. Cation transport in Escherichia coli. VIII. Potassium transport mutants. J Gen Physiol. 1976 Mar;67(3):325–341. doi: 10.1085/jgp.67.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Roth W. G., Porter S. E., Leckie M. P., Porter B. E., Dietzler D. N. Restoration of cell volume and the reversal of carbohydrate transport and growth inhibition of osmotically upshocked Escherichia coli. Biochem Biophys Res Commun. 1985 Jan 16;126(1):442–449. doi: 10.1016/0006-291x(85)90625-4. [DOI] [PubMed] [Google Scholar]
  24. Villarejo M., Davis J. L., Granett S. Osmoregulation of alkaline phosphatase synthesis in Escherichia coli K-12. J Bacteriol. 1983 Nov;156(2):975–978. doi: 10.1128/jb.156.2.975-978.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]

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

RESOURCES