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. 1996 Sep;178(17):5112–5120. doi: 10.1128/jb.178.17.5112-5120.1996

Identification of sigma S-regulated genes in Salmonella typhimurium: complementary regulatory interactions between sigma S and cyclic AMP receptor protein.

F C Fang 1, C Y Chen 1, D G Guiney 1, Y Xu 1
PMCID: PMC178306  PMID: 8752327

Abstract

sigma S (RpoS)-regulated lacZ transcriptional fusions in Salmonella typhimurium were identified from a MudJ transposon library by placing the rpoS gene under the control of the araBAD promoter and detecting lacZ expression in the presence or absence of arabinose supplementation. Western blot (immunoblot) analysis of bacteria carrying PBAD::rpoS demonstrated arabinose-dependent rpoS expression during all phases of growth. sigma S-dependent gene expression of individual gene fusions was confirmed by P22-mediated transduction of the MudJ insertions into wild-type or rpoS backgrounds. Analysis of six insertions revealed the known sigma S-regulated gene otsA, as well as five novel loci. Each of these genes is maximally expressed in stationary phase, and all but one show evidence of cyclic AMP receptor protein-dependent repression during logarithmic growth which is relieved in stationary phase. For these genes, as well as for the sigma S-regulated spvB plasmid virulence gene, a combination of rpoS overexpression and crp inactivation can result in high-level expression during logarithmic growth. The approach used to identify sigma S-regulated genes in this study provides a general method for the identification of genes controlled by trans-acting regulatory factors.

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Selected References

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

  1. Ailion M., Bobik T. A., Roth J. R. Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium. J Bacteriol. 1993 Nov;175(22):7200–7208. doi: 10.1128/jb.175.22.7200-7208.1993. [DOI] [PMC free article] [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. Altuvia S., Almirón M., Huisman G., Kolter R., Storz G. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol. 1994 Jul;13(2):265–272. doi: 10.1111/j.1365-2958.1994.tb00421.x. [DOI] [PubMed] [Google Scholar]
  4. Badger J. L., Miller V. L. Role of RpoS in survival of Yersinia enterocolitica to a variety of environmental stresses. J Bacteriol. 1995 Sep;177(18):5370–5373. doi: 10.1128/jb.177.18.5370-5373.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barth M., Marschall C., Muffler A., Fischer D., Hengge-Aronis R. Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sigma S and many sigma S-dependent genes in Escherichia coli. J Bacteriol. 1995 Jun;177(12):3455–3464. doi: 10.1128/jb.177.12.3455-3464.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bearson S. M., Benjamin W. H., Jr, Swords W. E., Foster J. W. Acid shock induction of RpoS is mediated by the mouse virulence gene mviA of Salmonella typhimurium. J Bacteriol. 1996 May;178(9):2572–2579. doi: 10.1128/jb.178.9.2572-2579.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Botsford J. L., Harman J. G. Cyclic AMP in prokaryotes. Microbiol Rev. 1992 Mar;56(1):100–122. doi: 10.1128/mr.56.1.100-122.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Böhringer J., Fischer D., Mosler G., Hengge-Aronis R. UDP-glucose is a potential intracellular signal molecule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli. J Bacteriol. 1995 Jan;177(2):413–422. doi: 10.1128/jb.177.2.413-422.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Castilho B. A., Olfson P., Casadaban M. J. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. doi: 10.1128/jb.158.2.488-495.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chang Y. Y., Wang A. Y., Cronan J. E., Jr Expression of Escherichia coli pyruvate oxidase (PoxB) depends on the sigma factor encoded by the rpoS(katF) gene. Mol Microbiol. 1994 Mar;11(6):1019–1028. doi: 10.1111/j.1365-2958.1994.tb00380.x. [DOI] [PubMed] [Google Scholar]
  12. Chen C. Y., Buchmeier N. A., Libby S., Fang F. C., Krause M., Guiney D. G. Central regulatory role for the RpoS sigma factor in expression of Salmonella dublin plasmid virulence genes. J Bacteriol. 1995 Sep;177(18):5303–5309. doi: 10.1128/jb.177.18.5303-5309.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Dorman C. J. 1995 Flemming Lecture. DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology. 1995 Jun;141(Pt 6):1271–1280. doi: 10.1099/13500872-141-6-1271. [DOI] [PubMed] [Google Scholar]
  15. Fang F. C., Krause M., Roudier C., Fierer J., Guiney D. G. Growth regulation of a Salmonella plasmid gene essential for virulence. J Bacteriol. 1991 Nov;173(21):6783–6789. doi: 10.1128/jb.173.21.6783-6789.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Fierer J., Eckmann L., Fang F., Pfeifer C., Finlay B. B., Guiney D. Expression of the Salmonella virulence plasmid gene spvB in cultured macrophages and nonphagocytic cells. Infect Immun. 1993 Dec;61(12):5231–5236. doi: 10.1128/iai.61.12.5231-5236.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fürste J. P., Pansegrau W., Frank R., Blöcker H., Scholz P., Bagdasarian M., Lanka E. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene. 1986;48(1):119–131. doi: 10.1016/0378-1119(86)90358-6. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Gerlach P., Søgaard-Andersen L., Pedersen H., Martinussen J., Valentin-Hansen P., Bremer E. The cyclic AMP (cAMP)-cAMP receptor protein complex functions both as an activator and as a corepressor at the tsx-p2 promoter of Escherichia coli K-12. J Bacteriol. 1991 Sep;173(17):5419–5430. doi: 10.1128/jb.173.17.5419-5430.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Guzman L. M., Belin D., Carson M. J., Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol. 1995 Jul;177(14):4121–4130. doi: 10.1128/jb.177.14.4121-4130.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hardesty C., Ferran C., DiRienzo J. M. Plasmid-mediated sucrose metabolism in Escherichia coli: characterization of scrY, the structural gene for a phosphoenolpyruvate-dependent sucrose phosphotransferase system outer membrane porin. J Bacteriol. 1991 Jan;173(2):449–456. doi: 10.1128/jb.173.2.449-456.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Hughes K. T., Roth J. R. Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics. 1988 May;119(1):9–12. doi: 10.1093/genetics/119.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Huisman G. W., Kolter R. Sensing starvation: a homoserine lactone--dependent signaling pathway in Escherichia coli. Science. 1994 Jul 22;265(5171):537–539. doi: 10.1126/science.7545940. [DOI] [PubMed] [Google Scholar]
  28. Itkor P., Tsukagoshi N., Udaka S. Nucleotide sequence of the raw-starch-digesting amylase gene from Bacillus sp. B1018 and its strong homology to the cyclodextrin glucanotransferase genes. Biochem Biophys Res Commun. 1990 Jan 30;166(2):630–636. doi: 10.1016/0006-291x(90)90855-h. [DOI] [PubMed] [Google Scholar]
  29. Jensen P. R., Loman L., Petra B., van der Weijden C., Westerhoff H. V. Energy buffering of DNA structure fails when Escherichia coli runs out of substrate. J Bacteriol. 1995 Jun;177(12):3420–3426. doi: 10.1128/jb.177.12.3420-3426.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Johnson C. M., Schleif R. F. In vivo induction kinetics of the arabinose promoters in Escherichia coli. J Bacteriol. 1995 Jun;177(12):3438–3442. doi: 10.1128/jb.177.12.3438-3442.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Josephsen J., Hammer-Jespersen K., Hansen T. D. Mapping of the gene for cytidine deaminase (cdd) in Escherichia coli K-12. J Bacteriol. 1983 Apr;154(1):72–75. doi: 10.1128/jb.154.1.72-75.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Kolodrubetz D., Schleif R. Regulation of the L-arabinose transport operons in Escherichia coli. J Mol Biol. 1981 Sep 15;151(2):215–227. doi: 10.1016/0022-2836(81)90512-x. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Krause M., Fang F. C., Guiney D. G. Regulation of plasmid virulence gene expression in Salmonella dublin involves an unusual operon structure. J Bacteriol. 1992 Jul;174(13):4482–4489. doi: 10.1128/jb.174.13.4482-4489.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Lange R., Fischer D., Hengge-Aronis R. Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J Bacteriol. 1995 Aug;177(16):4676–4680. doi: 10.1128/jb.177.16.4676-4680.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lange R., Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol. 1991 Jul;173(14):4474–4481. doi: 10.1128/jb.173.14.4474-4481.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. Lee I. S., Lin J., Hall H. K., Bearson B., Foster J. W. The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol. 1995 Jul;17(1):155–167. doi: 10.1111/j.1365-2958.1995.mmi_17010155.x. [DOI] [PubMed] [Google Scholar]
  42. Loewen P. C., Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. doi: 10.1146/annurev.mi.48.100194.000413. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. Marschall C., Hengge-Aronis R. Regulatory characteristics and promoter analysis of csiE, a stationary phase-inducible gene under the control of sigma S and the cAMP-CRP complex in Escherichia coli. Mol Microbiol. 1995 Oct;18(1):175–184. doi: 10.1111/j.1365-2958.1995.mmi_18010175.x. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. 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]
  49. Mead D. A., Skorupa E. S., Kemper B. Single stranded DNA SP6 promoter plasmids for engineering mutant RNAs and proteins: synthesis of a 'stretched' preproparathyroid hormone. Nucleic Acids Res. 1985 Feb 25;13(4):1103–1118. doi: 10.1093/nar/13.4.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Miksch G., Dobrowolski P. Growth phase-dependent induction of stationary-phase promoters of Escherichia coli in different gram-negative bacteria. J Bacteriol. 1995 Sep;177(18):5374–5378. doi: 10.1128/jb.177.18.5374-5378.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Muffler A., Fischer D., Altuvia S., Storz G., Hengge-Aronis R. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J. 1996 Mar 15;15(6):1333–1339. [PMC free article] [PubMed] [Google Scholar]
  52. 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]
  53. 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]
  54. Nguyen L. H., Jensen D. B., Thompson N. E., Gentry D. R., Burgess R. R. In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product. Biochemistry. 1993 Oct 19;32(41):11112–11117. doi: 10.1021/bi00092a021. [DOI] [PubMed] [Google Scholar]
  55. O'Byrne C. P., Dorman C. J. The spv virulence operon of Salmonella typhimurium LT2 is regulated negatively by the cyclic AMP (cAMP)-cAMP receptor protein system. J Bacteriol. 1994 Feb;176(3):905–912. doi: 10.1128/jb.176.3.905-912.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. O'Byrne C. P., Dorman C. J. Transcription of the Salmonella typhimurium spv virulence locus is regulated negatively by the nucleoid-associated protein H-NS. FEMS Microbiol Lett. 1994 Aug 1;121(1):99–105. doi: 10.1111/j.1574-6968.1994.tb07082.x. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. 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]
  59. Osuna R., Lienau D., Hughes K. T., Johnson R. C. Sequence, regulation, and functions of fis in Salmonella typhimurium. J Bacteriol. 1995 Apr;177(8):2021–2032. doi: 10.1128/jb.177.8.2021-2032.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Pratt L. A., Silhavy T. J. The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2488–2492. doi: 10.1073/pnas.93.6.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Prince R. W., Xu Y., Libby S. J., Fang F. C. Cloning and sequencing of the gene encoding the RpoS (KatF) sigma factor from Salmonella typhimurium 14028s. Biochim Biophys Acta. 1994 Sep 13;1219(1):198–200. doi: 10.1016/0167-4781(94)90271-2. [DOI] [PubMed] [Google Scholar]
  62. Robbe-Saule V., Coynault C., Norel F. The live oral typhoid vaccine Ty21a is a rpoS mutant and is susceptible to various environmental stresses. FEMS Microbiol Lett. 1995 Feb 15;126(2):171–176. doi: 10.1111/j.1574-6968.1995.tb07412.x. [DOI] [PubMed] [Google Scholar]
  63. Schultz J. E., Latter G. I., Matin A. Differential regulation by cyclic AMP of starvation protein synthesis in Escherichia coli. J Bacteriol. 1988 Sep;170(9):3903–3909. doi: 10.1128/jb.170.9.3903-3909.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schweder T., Lee K. H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol. 1996 Jan;178(2):470–476. doi: 10.1128/jb.178.2.470-476.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. 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]
  66. Spector M. P., Cubitt C. L. Starvation-inducible loci of Salmonella typhimurium: regulation and roles in starvation-survival. Mol Microbiol. 1992 Jun;6(11):1467–1476. doi: 10.1111/j.1365-2958.1992.tb00867.x. [DOI] [PubMed] [Google Scholar]
  67. 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]
  68. Tanaka K., Takahashi H. Cloning, analysis and expression of an rpoS homologue gene from Pseudomonas aeruginosa PAO1. Gene. 1994 Dec 2;150(1):81–85. doi: 10.1016/0378-1119(94)90862-1. [DOI] [PubMed] [Google Scholar]
  69. Touati E., Danchin A. The structure of the promoter and amino terminal region of the pH 2.5 acid phosphatase structural gene (appA) of E. coli: a negative control of transcription mediated by cyclic AMP. Biochimie. 1987 Mar;69(3):215–221. doi: 10.1016/0300-9084(87)90045-9. [DOI] [PubMed] [Google Scholar]
  70. Tuveson R. W., Jonas R. B. Genetic control of near-UV (300-400 NM) sensitivity independent of the recA gene in strains of Escherichia coli K12. Photochem Photobiol. 1979 Dec;30(6):667–676. doi: 10.1111/j.1751-1097.1979.tb07197.x. [DOI] [PubMed] [Google Scholar]
  71. 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]
  72. 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]
  73. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 1989 May 11;17(9):3469–3478. doi: 10.1093/nar/17.9.3469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Xu J., Johnson R. C. Fis activates the RpoS-dependent stationary-phase expression of proP in Escherichia coli. J Bacteriol. 1995 Sep;177(18):5222–5231. doi: 10.1128/jb.177.18.5222-5231.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Xu J., Johnson R. C. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol. 1995 Feb;177(4):938–947. doi: 10.1128/jb.177.4.938-947.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Xu J., Johnson R. C. aldB, an RpoS-dependent gene in Escherichia coli encoding an aldehyde dehydrogenase that is repressed by Fis and activated by Crp. J Bacteriol. 1995 Jun;177(11):3166–3175. doi: 10.1128/jb.177.11.3166-3175.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Yamashino T., Ueguchi C., Mizuno T. Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J. 1995 Feb 1;14(3):594–602. doi: 10.1002/j.1460-2075.1995.tb07035.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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