Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Feb;177(4):938–947. doi: 10.1128/jb.177.4.938-947.1995

Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli.

J Xu 1, R C Johnson 1
PMCID: PMC176687  PMID: 7860604

Abstract

Fis is a nucleoid-associated protein in Escherichia coli that has been shown to regulate recombination, replication, and transcription reactions. It is expressed in a transient manner under batch culturing conditions such that high levels are present during early exponential phase and low levels are present during late exponential phase and stationary phase. We have screened a random collection of transposon-induced lac fusions for those which give decreased expression in the presence of Fis. Thirteen different Fis-repressed genes were identified, including glnQ (glutamine high-affinity transport), mglA (methyl-galactoside transport), xylF (D-xylose-binding protein), sdhA (succinate dehydrogenase flavoprotein subunit), and a newly identified aldehyde dehydrogenase, aldB. The LacZ expression patterns revealed that many of the fusions were maximally expressed at different stages of growth, including early log phase, mid- to late log phase, and stationary phase. The expression of some of the late-exponential- and stationary-phase genes was dependent on the RpoS sigma factor, whereas that of others was affected negatively by RpoS. We conclude that Fis negatively regulates a diverse set of genes and that RpoS can function to both activate and inhibit the expression of specific genes.

Full Text

The Full Text of this article is available as a PDF (308.1 KB).

Selected References

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

  1. Almirón M., Link A. J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992 Dec;6(12B):2646–2654. doi: 10.1101/gad.6.12b.2646. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ball C. A., Osuna R., Ferguson K. C., Johnson R. C. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol. 1992 Dec;174(24):8043–8056. doi: 10.1128/jb.174.24.8043-8056.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buck M., Cannon W. Specific binding of the transcription factor sigma-54 to promoter DNA. Nature. 1992 Jul 30;358(6385):422–424. doi: 10.1038/358422a0. [DOI] [PubMed] [Google Scholar]
  6. Bétermier M., Poquet I., Alazard R., Chandler M. Involvement of Escherichia coli FIS protein in maintenance of bacteriophage mu lysogeny by the repressor: control of early transcription and inhibition of transposition. J Bacteriol. 1993 Jun;175(12):3798–3811. doi: 10.1128/jb.175.12.3798-3811.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Filutowicz M., Ross W., Wild J., Gourse R. L. Involvement of Fis protein in replication of the Escherichia coli chromosome. J Bacteriol. 1992 Jan;174(2):398–407. doi: 10.1128/jb.174.2.398-407.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Finkel S. E., Johnson R. C. The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol. 1992 Nov;6(22):3257–3265. doi: 10.1111/j.1365-2958.1992.tb02193.x. [DOI] [PubMed] [Google Scholar]
  9. Freundlich M., Ramani N., Mathew E., Sirko A., Tsui P. The role of integration host factor in gene expression in Escherichia coli. Mol Microbiol. 1992 Sep;6(18):2557–2563. doi: 10.1111/j.1365-2958.1992.tb01432.x. [DOI] [PubMed] [Google Scholar]
  10. Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., Cashel M. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J Bacteriol. 1993 Dec;175(24):7982–7989. doi: 10.1128/jb.175.24.7982-7989.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gille H., Egan J. B., Roth A., Messer W. The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli. Nucleic Acids Res. 1991 Aug 11;19(15):4167–4172. doi: 10.1093/nar/19.15.4167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gosink K. K., Ross W., Leirmo S., Osuna R., Finkel S. E., Johnson R. C., Gourse R. L. DNA binding and bending are necessary but not sufficient for Fis-dependent activation of rrnB P1. J Bacteriol. 1993 Mar;175(6):1580–1589. doi: 10.1128/jb.175.6.1580-1589.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Groisman E. A., Casadaban M. J. Mini-mu bacteriophage with plasmid replicons for in vivo cloning and lac gene fusing. J Bacteriol. 1986 Oct;168(1):357–364. doi: 10.1128/jb.168.1.357-364.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heim R., Strehler E. E. Cloning an Escherichia coli gene encoding a protein remarkably similar to mammalian aldehyde dehydrogenases. Gene. 1991 Mar 1;99(1):15–23. doi: 10.1016/0378-1119(91)90028-a. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Hogg R. W., Voelker C., Von Carlowitz I. Nucleotide sequence and analysis of the mgl operon of Escherichia coli K12. Mol Gen Genet. 1991 Oct;229(3):453–459. doi: 10.1007/BF00267469. [DOI] [PubMed] [Google Scholar]
  17. Iuchi S., Aristarkhov A., Dong J. M., Taylor J. S., Lin E. C. Effects of nitrate respiration on expression of the Arc-controlled operons encoding succinate dehydrogenase and flavin-linked L-lactate dehydrogenase. J Bacteriol. 1994 Mar;176(6):1695–1701. doi: 10.1128/jb.176.6.1695-1701.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson R. C., Bruist M. F., Simon M. I. Host protein requirements for in vitro site-specific DNA inversion. Cell. 1986 Aug 15;46(4):531–539. doi: 10.1016/0092-8674(86)90878-0. [DOI] [PubMed] [Google Scholar]
  19. Koch C., Kahmann R. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J Biol Chem. 1986 Nov 25;261(33):15673–15678. [PubMed] [Google Scholar]
  20. Koch C., Ninnemann O., Fuss H., Kahmann R. The N-terminal part of the E.coli DNA binding protein FIS is essential for stimulating site-specific DNA inversion but is not required for specific DNA binding. Nucleic Acids Res. 1991 Nov 11;19(21):5915–5922. doi: 10.1093/nar/19.21.5915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Kostrewa D., Granzin J., Koch C., Choe H. W., Raghunathan S., Wolf W., Labahn J., Kahmann R., Saenger W. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature. 1991 Jan 10;349(6305):178–180. doi: 10.1038/349178a0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. McCann M. P., Kidwell J. P., Matin A. The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol. 1991 Jul;173(13):4188–4194. doi: 10.1128/jb.173.13.4188-4194.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Mulvey M. R., Sorby P. A., Triggs-Raine B. L., Loewen P. C. Cloning and physical characterization of katE and katF required for catalase HPII expression in Escherichia coli. Gene. 1988 Dec 20;73(2):337–345. doi: 10.1016/0378-1119(88)90498-2. [DOI] [PubMed] [Google Scholar]
  27. Newlands J. T., Gaal T., Mecsas J., Gourse R. L. Transcription of the Escherichia coli rrnB P1 promoter by the heat shock RNA polymerase (E sigma 32) in vitro. J Bacteriol. 1993 Feb;175(3):661–668. doi: 10.1128/jb.175.3.661-668.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nilsson L., Emilsson V. Factor for inversion stimulation-dependent growth rate regulation of individual tRNA species in Escherichia coli. J Biol Chem. 1994 Apr 1;269(13):9460–9465. [PubMed] [Google Scholar]
  29. Nilsson L., Vanet A., Vijgenboom E., Bosch L. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 1990 Mar;9(3):727–734. doi: 10.1002/j.1460-2075.1990.tb08166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nilsson L., Verbeek H., Vijgenboom E., van Drunen C., Vanet A., Bosch L. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol. 1992 Feb;174(3):921–929. doi: 10.1128/jb.174.3.921-929.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ninnemann O., Koch C., Kahmann R. The E.coli fis promoter is subject to stringent control and autoregulation. EMBO J. 1992 Mar;11(3):1075–1083. doi: 10.1002/j.1460-2075.1992.tb05146.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nohno T., Saito T., Hong J. S. Cloning and complete nucleotide sequence of the Escherichia coli glutamine permease operon (glnHPQ). Mol Gen Genet. 1986 Nov;205(2):260–269. doi: 10.1007/BF00430437. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Osuna R., Finkel S. E., Johnson R. C. Identification of two functional regions in Fis: the N-terminus is required to promote Hin-mediated DNA inversion but not lambda excision. EMBO J. 1991 Jun;10(6):1593–1603. doi: 10.1002/j.1460-2075.1991.tb07680.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Priefert H., Krüger N., Jendrossek D., Schmidt B., Steinbüchel A. Identification and molecular characterization of the gene coding for acetaldehyde dehydrogenase II (acoD) of Alcaligenes eutrophus. J Bacteriol. 1992 Feb;174(3):899–907. doi: 10.1128/jb.174.3.899-907.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 1990 Nov;9(11):3733–3742. doi: 10.1002/j.1460-2075.1990.tb07586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sander P., Langert W., Mueller K. Mechanisms of upstream activation of the rrnD promoter P1 of Escherichia coli. J Biol Chem. 1993 Aug 15;268(23):16907–16916. [PubMed] [Google Scholar]
  38. Schmid M. B. More than just "histone-like" proteins. Cell. 1990 Nov 2;63(3):451–453. doi: 10.1016/0092-8674(90)90438-k. [DOI] [PubMed] [Google Scholar]
  39. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sofia H. J., Burland V., Daniels D. L., Plunkett G., 3rd, Blattner F. R. Analysis of the Escherichia coli genome. V. DNA sequence of the region from 76.0 to 81.5 minutes. Nucleic Acids Res. 1994 Jul 11;22(13):2576–2586. doi: 10.1093/nar/22.13.2576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Thompson J. F., Moitoso de Vargas L., Koch C., Kahmann R., Landy A. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell. 1987 Sep 11;50(6):901–908. doi: 10.1016/0092-8674(87)90516-2. [DOI] [PubMed] [Google Scholar]
  43. Wilmes-Riesenberg M. R., Wanner B. L. TnphoA and TnphoA' elements for making and switching fusions for study of transcription, translation, and cell surface localization. J Bacteriol. 1992 Jul;174(14):4558–4575. doi: 10.1128/jb.174.14.4558-4575.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wood D., Darlison M. G., Wilde R. J., Guest J. R. Nucleotide sequence encoding the flavoprotein and hydrophobic subunits of the succinate dehydrogenase of Escherichia coli. Biochem J. 1984 Sep 1;222(2):519–534. doi: 10.1042/bj2220519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yuan H. S., Finkel S. E., Feng J. A., Kaczor-Grzeskowiak M., Johnson R. C., Dickerson R. E. The molecular structure of wild-type and a mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9558–9562. doi: 10.1073/pnas.88.21.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES