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. 1996 Mar;178(5):1465–1468. doi: 10.1128/jb.178.5.1465-1468.1996

Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli?

L Notley 1, T Ferenci 1
PMCID: PMC177823  PMID: 8631726

Abstract

treA and osmY expression and RpoS protein levels were investigated in glucose-limited continuous culture. The level of induction of these stationary-phase markers became as high during growth at a D of 0.1 to 0.2 h(-1) as in carbon-starved batch cultures but only in rpoS+ bacteria. The stress protectant trehalose was actually produced at higher levels at low growth rates than in stationary-phase cultures. The pattern of induction of RpoS-dependent activities could be separated from those regulated by cyclic AMP (cAMP) or endoinduction, and the induction occurred at extreme glucose limitation. Escherichia coli turns to a protective stationary-phase response when nutrient levels fall below approximately 10(-7) M glucose, which is insufficient to saturate scavenger transporters regulated by cAMP plus endoinducers, and this response is optimally expressed at 10(-6) M glucose. The high-level induction of protective functions also explains the maintenance energy requirement of bacterial growth at low dilution rates.

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Selected References

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  1. Boos W., Ehmann U., Forkl H., Klein W., Rimmele M., Postma P. Trehalose transport and metabolism in Escherichia coli. J Bacteriol. 1990 Jun;172(6):3450–3461. doi: 10.1128/jb.172.6.3450-3461.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Death A., Ferenci T. Between feast and famine: endogenous inducer synthesis in the adaptation of Escherichia coli to growth with limiting carbohydrates. J Bacteriol. 1994 Aug;176(16):5101–5107. doi: 10.1128/jb.176.16.5101-5107.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Death A., Ferenci T. The importance of the binding-protein-dependent Mgl system to the transport of glucose in Escherichia coli growing on low sugar concentrations. Res Microbiol. 1993 Sep;144(7):529–537. doi: 10.1016/0923-2508(93)90002-j. [DOI] [PubMed] [Google Scholar]
  4. Death A., Notley L., Ferenci T. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol. 1993 Mar;175(5):1475–1483. doi: 10.1128/jb.175.5.1475-1483.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fang F. C., Libby S. J., Buchmeier N. A., Loewen P. C., Switala J., Harwood J., Guiney D. G. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11978–11982. doi: 10.1073/pnas.89.24.11978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Giaever H. M., Styrvold O. B., Kaasen I., Strøm A. R. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol. 1988 Jun;170(6):2841–2849. doi: 10.1128/jb.170.6.2841-2849.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Harder W., Dijkhuizen L. Physiological responses to nutrient limitation. Annu Rev Microbiol. 1983;37:1–23. doi: 10.1146/annurev.mi.37.100183.000245. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Kaasen I., Falkenberg P., Styrvold O. B., Strøm A. R. Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR) J Bacteriol. 1992 Feb;174(3):889–898. doi: 10.1128/jb.174.3.889-898.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kjelleberg S., Albertson N., Flärdh K., Holmquist L., Jouper-Jaan A., Marouga R., Ostling J., Svenblad B., Weichart D. How do non-differentiating bacteria adapt to starvation? Antonie Van Leeuwenhoek. 1993;63(3-4):333–341. doi: 10.1007/BF00871228. [DOI] [PubMed] [Google Scholar]
  13. Koch A. L. The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microb Physiol. 1971;6:147–217. doi: 10.1016/s0065-2911(08)60069-7. [DOI] [PubMed] [Google Scholar]
  14. Kolter R., Siegele D. A., Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol. 1993;47:855–874. doi: 10.1146/annurev.mi.47.100193.004231. [DOI] [PubMed] [Google Scholar]
  15. Kowarz L., Coynault C., Robbe-Saule V., Norel F. The Salmonella typhimurium katF (rpoS) gene: cloning, nucleotide sequence, and regulation of spvR and spvABCD virulence plasmid genes. J Bacteriol. 1994 Nov;176(22):6852–6860. doi: 10.1128/jb.176.22.6852-6860.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lange R., Barth M., Hengge-Aronis R. 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. J Bacteriol. 1993 Dec;175(24):7910–7917. doi: 10.1128/jb.175.24.7910-7917.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lange R., Hengge-Aronis R. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 1994 Jul 1;8(13):1600–1612. doi: 10.1101/gad.8.13.1600. [DOI] [PubMed] [Google Scholar]
  18. Manna D., Gowrishankar J. Evidence for involvement of proteins HU and RpoS in transcription of the osmoresponsive proU operon in Escherichia coli. J Bacteriol. 1994 Sep;176(17):5378–5384. doi: 10.1128/jb.176.17.5378-5384.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Notley L., Ferenci T. Differential expression of mal genes under cAMP and endogenous inducer control in nutrient-stressed Escherichia coli. Mol Microbiol. 1995 Apr;16(1):121–129. doi: 10.1111/j.1365-2958.1995.tb02397.x. [DOI] [PubMed] [Google Scholar]
  20. O'Neal C. R., Gabriel W. M., Turk A. K., Libby S. J., Fang F. C., Spector M. P. RpoS is necessary for both the positive and negative regulation of starvation survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium. J Bacteriol. 1994 Aug;176(15):4610–4616. doi: 10.1128/jb.176.15.4610-4616.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Pirt S. J. The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci. 1965 Oct 12;163(991):224–231. doi: 10.1098/rspb.1965.0069. [DOI] [PubMed] [Google Scholar]
  23. Raibaud O., Richet E. Maltotriose is the inducer of the maltose regulon of Escherichia coli. J Bacteriol. 1987 Jul;169(7):3059–3061. doi: 10.1128/jb.169.7.3059-3061.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Senn H., Lendenmann U., Snozzi M., Hamer G., Egli T. The growth of Escherichia coli in glucose-limited chemostat cultures: a re-examination of the kinetics. Biochim Biophys Acta. 1994 Dec 15;1201(3):424–436. doi: 10.1016/0304-4165(94)90072-8. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Strøm A. R., Kaasen I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol. 1993 Apr;8(2):205–210. doi: 10.1111/j.1365-2958.1993.tb01564.x. [DOI] [PubMed] [Google Scholar]
  28. Utsumi R., Kusafuka S., Nakayama T., Tanaka K., Takayanagi Y., Takahashi H., Noda M., Kawamukai M. Stationary phase-specific expression of the fic gene in Escherichia coli K-12 is controlled by the rpoS gene product (sigma 38). FEMS Microbiol Lett. 1993 Nov 1;113(3):273–278. doi: 10.1111/j.1574-6968.1993.tb06526.x. [DOI] [PubMed] [Google Scholar]
  29. Volkert M. R., Hajec L. I., Matijasevic Z., Fang F. C., Prince R. Induction of the Escherichia coli aidB gene under oxygen-limiting conditions requires a functional rpoS (katF) gene. J Bacteriol. 1994 Dec;176(24):7638–7645. doi: 10.1128/jb.176.24.7638-7645.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yim H. H., Brems R. L., Villarejo M. Molecular characterization of the promoter of osmY, an rpoS-dependent gene. J Bacteriol. 1994 Jan;176(1):100–107. doi: 10.1128/jb.176.1.100-107.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

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