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. 1996 Nov;178(22):6443–6450. doi: 10.1128/jb.178.22.6443-6450.1996

Role of the Escherichia coli FadR regulator in stasis survival and growth phase-dependent expression of the uspA, fad, and fab genes.

A Farewell 1, A A Diez 1, C C DiRusso 1, T Nyström 1
PMCID: PMC178529  PMID: 8932299

Abstract

The increased expression of the uspA gene of Escherichia coli is an essential part of the cell's response to growth arrest. We demonstrate that stationary-phase activation of the uspA promoter is in part dependent on growth phase-dependent inactivation or repression of the FadR regulator. Transcription of uspA is derepressed during exponential growth in fadR null mutants or by including the fatty acid oleate in the growth medium of FadR+ cells. The results of DNA footprinting analysis show that FadR binds downstream of the uspA promoter in the noncoding region. Thus, uspA is a member of the fadR regulon. All the fad-lacZ fusions examined (fadBA, fadL, and fadD) are increasingly expressed in stationary phase with kinetics similar to that of the increased expression of uspA. In contrast, beta-galactosidase levels decrease during stationary phase in a fabA-lacZ lysogen, consistent with the role of FadR as an activator of fabA. The growth phase-dependent increased and decreased transcription of fad genes and fabA, respectively, is dependent on the status of the fadR gene. Cells carrying a mutation in the FadR gene (fadRS219N) that makes it nonderepressible exhibit a weak stationary-phase induction of uspA and fad genes. In addition, cells carrying fadRS219N survive long-term stasis poorly, indicating that FadR-dependent alterations in fatty acid metabolism are an integral and important part of the adaptation to stationary phase.

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Selected References

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  1. Albertson N. H., Nyström T. Effects of starvation for exogenous carbon on functional mRNA stability and rate of peptide chain elongation in Escherichia coli. FEMS Microbiol Lett. 1994 Apr 1;117(2):181–187. doi: 10.1111/j.1574-6968.1994.tb06762.x. [DOI] [PubMed] [Google Scholar]
  2. Black P. N., DiRusso C. C. Molecular and biochemical analyses of fatty acid transport, metabolism, and gene regulation in Escherichia coli. Biochim Biophys Acta. 1994 Jan 3;1210(2):123–145. doi: 10.1016/0005-2760(94)90113-9. [DOI] [PubMed] [Google Scholar]
  3. DiRusso C. C., Heimert T. L., Metzger A. K. Characterization of FadR, a global transcriptional regulator of fatty acid metabolism in Escherichia coli. Interaction with the fadB promoter is prevented by long chain fatty acyl coenzyme A. J Biol Chem. 1992 Apr 25;267(12):8685–8691. [PubMed] [Google Scholar]
  4. DiRusso C. C., Metzger A. K., Heimert T. L. Regulation of transcription of genes required for fatty acid transport and unsaturated fatty acid biosynthesis in Escherichia coli by FadR. Mol Microbiol. 1993 Jan;7(2):311–322. doi: 10.1111/j.1365-2958.1993.tb01122.x. [DOI] [PubMed] [Google Scholar]
  5. Henry M. F., Cronan J. E., Jr Escherichia coli transcription factor that both activates fatty acid synthesis and represses fatty acid degradation. J Mol Biol. 1991 Dec 20;222(4):843–849. doi: 10.1016/0022-2836(91)90574-p. [DOI] [PubMed] [Google Scholar]
  6. Hiraoka S., Matsuzaki H., Shibuya I. Active increase in cardiolipin synthesis in the stationary growth phase and its physiological significance in Escherichia coli. FEBS Lett. 1993 Dec 27;336(2):221–224. doi: 10.1016/0014-5793(93)80807-7. [DOI] [PubMed] [Google Scholar]
  7. Hood M. A., Guckert J. B., White D. C., Deck F. Effect of nutrient deprivation on lipid, carbohydrate, DNA, RNA, and protein levels in Vibrio cholerae. Appl Environ Microbiol. 1986 Oct;52(4):788–793. doi: 10.1128/aem.52.4.788-793.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kokotek W., Lotz W. Construction of a lacZ-kanamycin-resistance cassette, useful for site-directed mutagenesis and as a promoter probe. Gene. 1989 Dec 14;84(2):467–471. doi: 10.1016/0378-1119(89)90522-2. [DOI] [PubMed] [Google Scholar]
  9. Linn T., St Pierre R. Improved vector system for constructing transcriptional fusions that ensures independent translation of lacZ. J Bacteriol. 1990 Feb;172(2):1077–1084. doi: 10.1128/jb.172.2.1077-1084.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Magnuson K., Jackowski S., Rock C. O., Cronan J. E., Jr Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol Rev. 1993 Sep;57(3):522–542. doi: 10.1128/mr.57.3.522-542.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Nyström T., Neidhardt F. C. Cloning, mapping and nucleotide sequencing of a gene encoding a universal stress protein in Escherichia coli. Mol Microbiol. 1992 Nov;6(21):3187–3198. doi: 10.1111/j.1365-2958.1992.tb01774.x. [DOI] [PubMed] [Google Scholar]
  12. Nyström T., Neidhardt F. C. Effects of overproducing the universal stress protein, UspA, in Escherichia coli K-12. J Bacteriol. 1996 Feb;178(3):927–930. doi: 10.1128/jb.178.3.927-930.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Nyström T., Neidhardt F. C. Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol Microbiol. 1994 Feb;11(3):537–544. doi: 10.1111/j.1365-2958.1994.tb00334.x. [DOI] [PubMed] [Google Scholar]
  14. Nyström T., Neidhardt F. C. Isolation and properties of a mutant of Escherichia coli with an insertional inactivation of the uspA gene, which encodes a universal stress protein. J Bacteriol. 1993 Jul;175(13):3949–3956. doi: 10.1128/jb.175.13.3949-3956.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nyström T. The trials and tribulations of growth arrest. Trends Microbiol. 1995 Apr;3(4):131–136. doi: 10.1016/s0966-842x(00)88901-5. [DOI] [PubMed] [Google Scholar]
  16. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  17. Raman N., DiRusso C. C. Analysis of acyl coenzyme A binding to the transcription factor FadR and identification of amino acid residues in the carboxyl terminus required for ligand binding. J Biol Chem. 1995 Jan 20;270(3):1092–1097. doi: 10.1074/jbc.270.3.1092. [DOI] [PubMed] [Google Scholar]
  18. Reeve C. A., Amy P. S., Matin A. Role of protein synthesis in the survival of carbon-starved Escherichia coli K-12. J Bacteriol. 1984 Dec;160(3):1041–1046. doi: 10.1128/jb.160.3.1041-1046.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  20. VanBogelen R. A., Neidhardt F. C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589–5593. doi: 10.1073/pnas.87.15.5589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Vanderwinkel E., De Vlieghere M., Fontaine M., Charles D., Denamur F., Vandevoorde D., De Kegel D. Septation deficiency and phosphilipid perturbation in Escherichia coli genetically constitutive for the beta oxidation pathway. J Bacteriol. 1976 Sep;127(3):1389–1399. doi: 10.1128/jb.127.3.1389-1399.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

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