Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Dec;175(24):7910–7917. doi: 10.1128/jb.175.24.7910-7917.1993

Complex transcriptional control of the sigma s-dependent stationary-phase-induced and osmotically regulated osmY (csi-5) gene suggests novel roles for Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex, and integration host factor in the stationary-phase response of Escherichia coli.

R Lange 1, M Barth 1, R Hengge-Aronis 1
PMCID: PMC206969  PMID: 8253679

Abstract

osmY (csi-5) is a representative of a large group of sigma s-dependent genes in Escherichia coli that exhibit both stationary-phase induction and osmotic regulation. A chromosomal transcriptional lacZ fusion (csi-5::lacZ) was used to study the regulation of osmY. We show here that in addition to sigma s, the global regulators Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex (cAMP-CRP), and integration host factor (IHF) are involved in the control of osmY. All three regulators negatively modulate the expression of osmY, and they act independently from sigma s. Stationary-phase induction of osmY in minimal medium can be explained by stimulation by sigma s combined with a relief of Lrp repression. Stationary-phase induction of osmY in rich medium is mediated by the combined action of sigma s, Lrp, cAMP-CRP, and IHF, with the latter three proteins acting as transition state regulators. The transcriptional start site of osmY was determined and revealed an mRNA with an unusual long nontranslated leader of 244 nucleotides. The regulatory region is characterized by a sigma 70-like -10 promoter region and contains potential binding sites for Lrp, CRP, and IHF. Whereas sigma s, Lrp, CRP, and IHF are clearly involved in stationary-phase induction, none of these regulators is essential for osmotic regulation of osmY.

Full text

PDF
7910

Images in this article

7914Image
on p.7914

Selected References

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

  1. Andrews J. C., Blevins T. C., Short S. A. Regulation of peptide transport in Escherichia coli: induction of the trp-linked operon encoding the oligopeptide permease. J Bacteriol. 1986 Feb;165(2):428–433. doi: 10.1128/jb.165.2.428-433.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atlung T., Nielsen A., Hansen F. G. Isolation, characterization, and nucleotide sequence of appY, a regulatory gene for growth-phase-dependent gene expression in Escherichia coli. J Bacteriol. 1989 Mar;171(3):1683–1691. doi: 10.1128/jb.171.3.1683-1691.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benner D., Müller N., Boos W. Temperature-sensitive catabolite activator protein in Escherichia coli BUG6. J Bacteriol. 1985 Jan;161(1):347–352. doi: 10.1128/jb.161.1.347-352.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. II. The binding specificity of cyclic AMP receptor protein to recognition sites. J Mol Biol. 1988 Apr 20;200(4):709–723. doi: 10.1016/0022-2836(88)90482-2. [DOI] [PubMed] [Google Scholar]
  5. Blum P. H., Jovanovich S. B., McCann M. P., Schultz J. E., Lesley S. A., Burgess R. R., Matin A. Cloning and in vivo and in vitro regulation of cyclic AMP-dependent carbon starvation genes from Escherichia coli. J Bacteriol. 1990 Jul;172(7):3813–3820. doi: 10.1128/jb.172.7.3813-3820.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Buettner M. J., Spitz E., Rickenberg H. V. Cyclic adenosine 3',5'-monophosphate in Escherichia coli. J Bacteriol. 1973 Jun;114(3):1068–1073. doi: 10.1128/jb.114.3.1068-1073.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chuang S. E., Daniels D. L., Blattner F. R. Global regulation of gene expression in Escherichia coli. J Bacteriol. 1993 Apr;175(7):2026–2036. doi: 10.1128/jb.175.7.2026-2036.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Collado-Vides J., Magasanik B., Gralla J. D. Control site location and transcriptional regulation in Escherichia coli. Microbiol Rev. 1991 Sep;55(3):371–394. doi: 10.1128/mr.55.3.371-394.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. D'Ari R., Lin R. T., Newman E. B. The leucine-responsive regulatory protein: more than a regulator? Trends Biochem Sci. 1993 Jul;18(7):260–263. doi: 10.1016/0968-0004(93)90177-o. [DOI] [PubMed] [Google Scholar]
  11. Dassa J., Fsihi H., Marck C., Dion M., Kieffer-Bontemps M., Boquet P. L. A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA) Mol Gen Genet. 1991 Oct;229(3):341–352. doi: 10.1007/BF00267454. [DOI] [PubMed] [Google Scholar]
  12. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ernsting B. R., Atkinson M. R., Ninfa A. J., Matthews R. G. Characterization of the regulon controlled by the leucine-responsive regulatory protein in Escherichia coli. J Bacteriol. 1992 Feb;174(4):1109–1118. doi: 10.1128/jb.174.4.1109-1118.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gamas P., Burger A. C., Churchward G., Caro L., Galas D., Chandler M. Replication of pSC101: effects of mutations in the E. coli DNA binding protein IHF. Mol Gen Genet. 1986 Jul;204(1):85–89. doi: 10.1007/BF00330192. [DOI] [PubMed] [Google Scholar]
  15. Groat R. G., Schultz J. E., Zychlinsky E., Bockman A., Matin A. Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival. J Bacteriol. 1986 Nov;168(2):486–493. doi: 10.1128/jb.168.2.486-493.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Haney S. A., Platko J. V., Oxender D. L., Calvo J. M. Lrp, a leucine-responsive protein, regulates branched-chain amino acid transport genes in Escherichia coli. J Bacteriol. 1992 Jan;174(1):108–115. doi: 10.1128/jb.174.1.108-115.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hengge-Aronis R., Fischer D. Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1877–1886. doi: 10.1111/j.1365-2958.1992.tb01360.x. [DOI] [PubMed] [Google Scholar]
  18. Hengge-Aronis R., Klein W., Lange R., Rimmele M., Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991 Dec;173(24):7918–7924. doi: 10.1128/jb.173.24.7918-7924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hengge-Aronis R., Lange R., Henneberg N., Fischer D. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol. 1993 Jan;175(1):259–265. doi: 10.1128/jb.175.1.259-265.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  22. Lange R., Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):49–59. doi: 10.1111/j.1365-2958.1991.tb01825.x. [DOI] [PubMed] [Google Scholar]
  23. Lin R., D'Ari R., Newman E. B. Lambda placMu insertions in genes of the leucine regulon: extension of the regulon to genes not regulated by leucine. J Bacteriol. 1992 Mar;174(6):1948–1955. doi: 10.1128/jb.174.6.1948-1955.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Loewen P. C., von Ossowski I., Switala J., Mulvey M. R. KatF (sigma S) synthesis in Escherichia coli is subject to posttranscriptional regulation. J Bacteriol. 1993 Apr;175(7):2150–2153. doi: 10.1128/jb.175.7.2150-2153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lonetto M., Gribskov M., Gross C. A. The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol. 1992 Jun;174(12):3843–3849. doi: 10.1128/jb.174.12.3843-3849.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matin A. The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):3–10. doi: 10.1111/j.1365-2958.1991.tb01819.x. [DOI] [PubMed] [Google Scholar]
  27. McCann M. P., Fraley C. D., Matin A. The putative sigma factor KatF is regulated posttranscriptionally during carbon starvation. J Bacteriol. 1993 Apr;175(7):2143–2149. doi: 10.1128/jb.175.7.2143-2149.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mulvey M. R., Loewen P. C. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res. 1989 Dec 11;17(23):9979–9991. doi: 10.1093/nar/17.23.9979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mulvey M. R., Switala J., Borys A., Loewen P. C. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol. 1990 Dec;172(12):6713–6720. doi: 10.1128/jb.172.12.6713-6720.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Newman E. B., D'Ari R., Lin R. T. The leucine-Lrp regulon in E. coli: a global response in search of a raison d'être. Cell. 1992 Feb 21;68(4):617–619. doi: 10.1016/0092-8674(92)90135-y. [DOI] [PubMed] [Google Scholar]
  31. Olsén A., Arnqvist A., Hammar M., Sukupolvi S., Normark S. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol. 1993 Feb;7(4):523–536. doi: 10.1111/j.1365-2958.1993.tb01143.x. [DOI] [PubMed] [Google Scholar]
  32. Platko J. V., Willins D. A., Calvo J. M. The ilvIH operon of Escherichia coli is positively regulated. J Bacteriol. 1990 Aug;172(8):4563–4570. doi: 10.1128/jb.172.8.4563-4570.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schellhorn H. E., Hassan H. M. Transcriptional regulation of katE in Escherichia coli K-12. J Bacteriol. 1988 Sep;170(9):4286–4292. doi: 10.1128/jb.170.9.4286-4292.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schultz J. E., Matin A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli. J Mol Biol. 1991 Mar 5;218(1):129–140. doi: 10.1016/0022-2836(91)90879-b. [DOI] [PubMed] [Google Scholar]
  35. Siegele D. A., Kolter R. Life after log. J Bacteriol. 1992 Jan;174(2):345–348. doi: 10.1128/jb.174.2.345-348.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Strauch M. A., Hoch J. A. Transition-state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol Microbiol. 1993 Feb;7(3):337–342. doi: 10.1111/j.1365-2958.1993.tb01125.x. [DOI] [PubMed] [Google Scholar]
  37. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3511–3515. doi: 10.1073/pnas.90.8.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tuan L. R., D'Ari R., Newman E. B. The leucine regulon of Escherichia coli K-12: a mutation in rblA alters expression of L-leucine-dependent metabolic operons. J Bacteriol. 1990 Aug;172(8):4529–4535. doi: 10.1128/jb.172.8.4529-4535.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wang Q., Calvo J. M. Lrp, a global regulatory protein of Escherichia coli, binds co-operatively to multiple sites and activates transcription of ilvIH. J Mol Biol. 1993 Jan 20;229(2):306–318. doi: 10.1006/jmbi.1993.1036. [DOI] [PubMed] [Google Scholar]
  40. Weichart D., Lange R., Henneberg N., Hengge-Aronis R. Identification and characterization of stationary phase-inducible genes in Escherichia coli. Mol Microbiol. 1993 Oct;10(2):407–420. [PubMed] [Google Scholar]
  41. Yim H. H., Villarejo M. osmY, a new hyperosmotically inducible gene, encodes a periplasmic protein in Escherichia coli. J Bacteriol. 1992 Jun;174(11):3637–3644. doi: 10.1128/jb.174.11.3637-3644.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES