Skip to main content
NCBI home page
Science Progress logoLink to Science Progress
. 2019 Feb 27;90(2-3):103–127. doi: 10.3184/003685007X215922

The σS subunit of RNA polymerase as a signal integrator and network master regulator in the general stress response in Escherichia coli

Eberhard Klauck 1, Athanasios Typas 2, Regine Hengge 3,✉
PMCID: PMC10368345  PMID: 17725229

Abstract

The σS (RpoS) subunit of RNA polymerase in Escherichia coli is a key master regulator which allows this bacterial model organism and important pathogen to adapt to and survive environmentally rough times. While hardly present in rapidly growing cells, σS strongly accumulates in response to many different stress conditions, partly replaces the vegetative sigma subunit in RNA polymerase and thereby reprograms this enzyme to transcribe σS-dependent genes (up to 10% of the E. coli genes). In this review, we summarize the extremely complex regulation of σS itself and multiple signal input at the level of this master regulator, we describe the way in which σS specifically recognizes “stress” promoters despite their similarity to vegetative promoters, and, while being far from comprehensive, we give a short overview of the far-reaching physiological impact of σS. With σS being a central and multiple signal integrator and master regulator of hundreds of genes organized in regulatory cascades and sub-networks or regulatory modules, this system also represents a key model system for analyzing complex cellular information processing and a starting point for understanding the complete regulatory network of an entire cell.

Keywords: bacterial stress responses, regulatory networks, signal transduction, post-transcriptional regulation, starvation

Full Text

The Full Text of this article is available as a PDF (368.1 KB).

References

  • 1.Hengge-Aronis R. (2002) Signal transduction and regulatory mechanisms involved in control of the σS subunit of RNA polymerase in Escherichia coli. Microbiol. Molec. Biol. Rev., 66, 373–395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Weber H., Polen T., Heuveling J., Wendisch V., and Hengge R. (2005) Genome-wide analysis of the general stress response network in Escherichia colt σS-dependent genes, promoters and sigma factor selectivity. J. Bacterial., 187, 1591–1603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Hengge-Aronis R. (2002) Stationary phase gene regulation: what makes an Escherichia coli promoter σS-dependent? Curr. Op. Microbiol., 5, 591–595. [DOI] [PubMed] [Google Scholar]
  • 4.Typas A., Becker G., and Hengge R. (2007) The molecular basis of selective promoter activation by the σS-subunit of RNA polymerase. Mol. Microbiol., 63, 1296–1306. [DOI] [PubMed] [Google Scholar]
  • 5.Lange R., and Hengge-Aronis R. (1994) The nlpD gene is located in an operon with rpoS on the Escherichia coli chromosome and encodes a novel lipoprotein with a potential function in cell wall formation. Mol. Microbiol., 13, 733–743. [DOI] [PubMed] [Google Scholar]
  • 6.Lange R., Fischer D., and Hengge-Aronis R. (1995) Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the σS subunit of RNA-polymerase in Escherichia coli. J. Bacteriol., 177, 4676–4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Lange R., and Hengge-Aronis R. (1994) The cellular concentration of the σS subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev., 8, 1600–1612. [DOI] [PubMed] [Google Scholar]
  • 8.Liu M. et al. (2005) Global transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. J. Biol. Chem., 280, 15921–15927. [DOI] [PubMed] [Google Scholar]
  • 9.Teich A. et al. (1999) Growth rate related concentration changes of the starvation response regulators σS and ppGpp in glucose-limited fed-batch and continuous cultures of Escherichia coli. Biotechnol. Progr., 15, 123–129. [DOI] [PubMed] [Google Scholar]
  • 10.Ihssen J., and Egli T. (2004) Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology, 150, 1637–1648. [DOI] [PubMed] [Google Scholar]
  • 11.Notley L., and Ferenci T. (1996) Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli. J. Bacteriol., 178, 1465–1468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Lange R., and Hengge-Aronis R. (1991) Growth phase-regulated expression of bolA and morphology of stationary phase Escherichia coli cells is controlled by the novel sigma factor σS (rpoS). J. Bacteriol., 173, 4474–4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Mika F., and Hengge R. (2005) A two-component phosphotransfer network involving ArcB, ArcA and RssB coordinates synthesis and proteolysis of σS in E. coli. Genes Dev., 19, 2770–2781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Pernestig A.-K. et al. (2003) The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J. Bacteriol., 185, 843–853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Teplitski M., Goodier R. I., and Ahmer B. M. (2003) Pathways heading from BarA/SirA to motility and virulence gene expression in Salmonella. J. Bacteriol., 185, 7257–7265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Tomenius H. et al. (2006) The Escherichia coli BarA-UvrY two-component system is a virulence determinant in the urinary tract. BMC Microbiol., 6, 27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Herren C. et al. (2006) The BarA-UvrY two-component system regulates virulence in avian pathogenic Escherichia coli 078: K80: H9. Infect. Immunol., 74, 4900–4909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Mukhopadhyay S., Audia J. P., Roy R. N., and Schellhorn H. E. (2000) Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol. Microbiol., 37, 371–381. [DOI] [PubMed] [Google Scholar]
  • 19.Sugiura M., Aiba H., and Mizuno T. (2003) Identification and classification of two-component systems that affect rpoS expression in Escherichia coli. Biosci. Biotechnol. Biochem., 67, 1612–1615. [DOI] [PubMed] [Google Scholar]
  • 20.Georgellis D., Kwon O., and Lin E. C. C. (2001) Quinones as the redox signal for the Arc Two-component system of bacteria. Science, 292, 2314–2315. [DOI] [PubMed] [Google Scholar]
  • 21.Azam T. A., Iwata A., Nishimura A., Ueda S., and Ishihama A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol., 181, 6361–6370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Hirsch M., and Elliott T. (2005) Fis regulates transcriptional induction of RpoS in Salmonella enterica. J. Bacterial., 187, 1568–1580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Crooke E., Akiyama M., Rao N. N., and Kornberg A. (1994) Genetically altered levels of inorganic polyphosphate in Escherichia coli. J. Biol. Chem., 269, 6290–6295. [PubMed] [Google Scholar]
  • 24.Rao N. N., and Kornberg A. (1996) Inorganic polyphosphate supports resistance can survival of stationary-phase Escherichia coli. J. Bacteriol., 178, 1394–1400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Shiba T. et al. (1997) Inorganic polyphosphate and the induction of rpoS expression. Proc. Natl. Acac. Sci. USA, 94, 11210–11215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Magnusson L. U., Farewell A., and Nyström T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol., 13, 236–242. [DOI] [PubMed] [Google Scholar]
  • 27.Cashel M., Gentry D. R., Hernandez V. J., and Vinella D. (1996) In: Neidhardt F.C.e.a. (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. pp. 1458–1496. ASM Press, Washington D.C. [Google Scholar]
  • 28.Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., and Cashel M. (1993) Synthesis of the stationary-phase sigma factor sS is positively regulated by ppGpp. J. Bacteriol., 175, 7982–7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Hirsch M., and Elliott T. (2002) Role of ppGpp in rpoS Stationary-Phase Regulation in Escherichia coli. J. Bacteriol., 184, 5077–5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Brown L., and Elliott T. (1997) Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J. Bacteriol., 179, 656–662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Cunning C., and Elliott T. (1999) RpoS synthesis is growth rate regulated in Salmonella typhimurium but its turnover is not dependent on acetyl phosphate synthesis or PTS function. J. Bacteriol., 181, 4853–4862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Hirsch M., and Elliott T. (2005) Stationary-phase regulation of RpoS translation in Escherichia coli. J. Bacteriol., 187, 7204–7213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Lease R. A., Cusick M. E., and Beifort M. (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA: RNA interaction at multiple loci. Proc. Natl. Acad. Sci. USA, 95, 12456–12461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Majdalani N., Cunning C., Sledjeski D., Elliott T., and Gottesman S. (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanims, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. USA, 95, 12462–12467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Muffler A., Traulsen D. D., Lange R., and Hengge-Aronis R. (1996) Posttranscriptional osmotic regulation of the σS subunit of RNA polymerase in Escherichia coli. J. Bacteriol., 178, 1607–1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Lee I. S., Lin J., Hall H. K., Bearson B., and Foster J. W. (1995) The stationary-phase sigma factor σS (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol. Microbiol., 17, 155–167. [DOI] [PubMed] [Google Scholar]
  • 37.Repoila F., Majdalani N., and Gottesman S. (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol. Microbiol., 48, 855–861. [DOI] [PubMed] [Google Scholar]
  • 38.Valentin-Hansen P., Eriksen M., and Udesen C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol., 51, 1525–1533. [DOI] [PubMed] [Google Scholar]
  • 39.Muffler A., Fischer D., and Hengge-Aronis R. (1996) The RNA-binding protein HF-I, known as a host factor for phage Qβ RNA replication, is essential for the translational regulation of rpoS in Escherichia coli. Genes Dev., 10, 1143–1151. [DOI] [PubMed] [Google Scholar]
  • 40.Brown L., and Elliott T. (1996) Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J. Bacteriol., 178, 3763–3770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Sauter C. (2003) Sm-like protein in eubacteria: the crystal structure of the Hfq protein from Escherichia coli. Nucl. Acids Res., 31, 4091–4098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Schumacher M.A. (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J., 21, 3546–3556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Majdalani N., Chen S., Murrow J., St. John K., and Gottesman S. (2001) Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol. Microbiol., 39, 1382–1394. [DOI] [PubMed] [Google Scholar]
  • 44.Majdalani N., Hernandez D., and Gottesman S. (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol., 46, 813–826. [DOI] [PubMed] [Google Scholar]
  • 45.Sledjeski D. D., Gupta A., and Gottesman S. (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in E. coli. EMBO J., 15, 3993–4000. [PMC free article] [PubMed] [Google Scholar]
  • 46.Koleva R. I. et al. (2006) Interactions of ribosomal protein S1 with DsrA and rpoS mRNA. BBRC, 348, 662–668. [DOI] [PubMed] [Google Scholar]
  • 47.Zhang A. et al. (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J., 17, 6061–6068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Altuvia S., Weinstein-Fischer D., Zhang A., Postow L., and Storz G. (1997) A small, stable RNA induced by oxidative stress: roles as a pleiotropic regulator and antimutator. Cell, 90, 43–53. [DOI] [PubMed] [Google Scholar]
  • 49.Balandina A., Claret L., Hengge-Aronis R., and Rouvière-Yaniv J. (2001) The Escherichia coli histone-like protein HU regulates rpoS translation. Mol. Microbiol., 39, 1069–1079. [DOI] [PubMed] [Google Scholar]
  • 50.Barth M., Marschall C., Muffler A., Fischer D., and Hengge-Aronis R. (1995) A role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of σS and many σS-dependent genes in Escherichia coli. J. Bacteriol., 177, 3455–3464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Yamashino T., Ueguchi C., and Mizuno T. (1995) Quantitative control of the stationary phase-specific sigma factor, σS, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J., 14, 594–602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Dorman C. J. (2004) H-NS: a universal regulator for a dynamic genome. Nature Rev. Microbiol., 2, 391–400. [DOI] [PubMed] [Google Scholar]
  • 53.Brescia C., Kaw M., and Sledjeski D. (2004) The DNA binding protein H-NS binds to and alters the stability of RNA in vitro and in vivo. J. Mol. Biol., 339, 505–514. [DOI] [PubMed] [Google Scholar]
  • 54.Klauck E., Böhringer J., and Hengge-Aronis R. (1997) The LysR-like regulator LeuO in Escherichia coli is involved in the translational regulation of rpoS by affecting the expression of the small regulatory DsrA-RNA. Mol. Microbiol., 25, 559–569. [DOI] [PubMed] [Google Scholar]
  • 55.Repoila F., and Gottesman S. (2001) Signal transduction cascade for regulation of rpoS: temperature regulation of dsrA. J. Bacteriol., 183, 4012–4023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Peterson C. N., Carabetta V. J., Chowdhury T., and Silhavy T. J. (2006) LrhA regulates rpoS translation in response to the Rcs phosphorelay system in Escherichia coli. J. Bacteriol., 188, 3175–3181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Huang Y., Ferrieres L., and Clarke D. (2006) The role of the Rcs phosphorelay in Enterobacteriaceae. Res. Microbiol., 157, 206–212. [DOI] [PubMed] [Google Scholar]
  • 58.Majdalani N., and Gottesman S. (2005) The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol., 599, 379–405. [DOI] [PubMed] [Google Scholar]
  • 59.Muffler A., Barth M., Marschall C., and Hengge-Aronis R. (1997) Heat shock regulation of σS turnover: a role for DnaK and relationship between stress responses mediated by σS and σ32 in Escherichia coli. J. Bacteriol., 179, 445–452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Rockabrand D. et al. (1998) Roles of DnaK and RpoS in starvation-induced thermotolerance of Escherichia coli. J. Bacteriol., 180, 846–854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Ueguchi C., Misonou N., and Mizuno T. (2001) Negative control of rpoS expression by phosphoenolpyruvate: carbohydrate phosphotransferase system in Escherichia coli. J. Bacteriol., 183, 520–527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Paul B. J. et al. (2004) DksA: a critical component of the transcriptiona initiation machinery that potentiates the regulation or rRNA promoters by ppGpp and the initiating NTP. Cell, 118, 311–322. [DOI] [PubMed] [Google Scholar]
  • 63.Paul B. J., Berkmen M., and Course R. L. (2005) DksA potentiates direct activation of amino acid promoters by ppGpp. Proc. Natl. Acad. Sci. USA, 102, 7823–7828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Webb C., Moreno M., Wilmes-Riesenberg M., Curtiss R. III, and Foster J. W. (1999) Effects of DksA and ClpP protease on sigma S production and virulence in Salmonella typhimurium. Mol. Microbiol., 34, 112–123. [DOI] [PubMed] [Google Scholar]
  • 65.Jenal U., and Hengge-Aronis R. (2003) Regulation by proteolysis in bacterial cells. Curr. Opin. Microbiol., 6, 163–172. [DOI] [PubMed] [Google Scholar]
  • 66.Schweder T., Lee K.-H., Lomovskaya O., and Matin A. (1996) Regulation of Escherichia coli starvation sigma factor (σS) by ClpXP protease. J. Bacteriol., 178, 470–476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Muffler A., Fischer D., Altuvia S., Storz G., and Hengge-Aronis R. (1996) The response regulator RssB controls stability of the σS subunit of RNA polymerase in Escherichia coli. EMBO J., 15, 1333–1339. [PMC free article] [PubMed] [Google Scholar]
  • 68.Pratt L. A., and Silhavy T. J. (1996) The response regulator, SprE, controls the stability of RpoS. Proc. Natl. Acad. Sci. USA, 93, 2488–2492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Bouché S. et al. (1998) Regulation of RssB-dependent proteolysis in Escherichia coli: a role for acetyl phosphate in a response regulator-controlled process. Mol. Microbiol., 27, 787–795. [DOI] [PubMed] [Google Scholar]
  • 70.Klauck E., Lingnau M., and Hengge-Aronis R. (2001) Role of the response regulator RssB in σS recognition and initiation of σS proteolysis in Escherichia coli. Mol. Microbiol., 40, 1381–1390. [DOI] [PubMed] [Google Scholar]
  • 71.Zhou Y., Gottesman S., Hoskins J. R., Maurizi M. R., and Wickner S. (2001) The RssB response regulator directly targets σS for degradation by ClpXP. Genes Dev., 15, 627–637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Becker G., Klauck E., and Hengge-Aronis R. (1999) Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl. Acad. Sci. USA, 96, 6439–6444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Becker G., and Hengge-Aronis R. (2001) What makes an Escherichia coli promoter σS-dependent? Role of the -13/-14 nucleotide promoter positions and region 2.5 of σS. Mol. Microbiol., 39, 1153–1165. [DOI] [PubMed] [Google Scholar]
  • 74.Campbell E. A. et al. (2002) Structure of the bacterial RNA polymerase promoter specificity a subunit. Mol. Cell, 9, 527–539. [DOI] [PubMed] [Google Scholar]
  • 75.Stüdemann A. et al. (2003) Sequential recognition of two distinct sites in σS by the proteolytic targeting factor RssB and ClpX. EMBO J., 22, 4111–4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Peterson C. N., Ruiz N., and Silhavy T. J. (2004) RpoS proteolysis is regulated by a mechanism that does not require the SprE (RssB) response regulator phosphorylation site. J. Bacteriol., 186, 7403–7410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Pruteanu M., and Hengge-Aronis R. (2002) The cellular level of the recognition factor RssB is rate-limiting for σS proteolysis: Implications for RssB regulation and signal transduction in σS turnover in Escherichia coli. Mol. Microbiol., 45, 1701–1714. [DOI] [PubMed] [Google Scholar]
  • 78.Zhou A. N., and Gottesman S. (1998) Regulation of proteolysis of the stationary-phase sigma factor RpoS. J. Bacteriol., 180, 1154–1158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Yamamoto K. et al. (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem., 280, 1448–1456. [DOI] [PubMed] [Google Scholar]
  • 80.Malpica R., Sandoval G. R., Rodriguez C., Franco B., and Georgellis D. (2006) Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid. Redox Signal., 8, 781–795. [DOI] [PubMed] [Google Scholar]
  • 81.Malpica R., Franco B., Rodriguez C., Kwon O., and Georgellis D. (2004) Identification of quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. USA, 101, 13318–13323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Hengge R. (2007) In: Utsumi R. (ed.), Bacterial Signal Transduction: Network and Drug Targets. (in press) (Landes Bioscience; ). [Google Scholar]
  • 83.Becker G., Klauck E., and Hengge-Aronis R. (2000) The response regulator RssB, a recognition factor for σS proteolysis in Escherichia coli, can act like an anti-σS factor. Mol. Microbiol., 35, 657–666. [DOI] [PubMed] [Google Scholar]
  • 84.Bougdour A., Wickner S., and Gottesman S. (2006) Modulating RssB activity: IraP, a novel regulator of σS stability in Escherichia coli. Genes Dev., 20, 884–897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85.Groisman E. A. (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol., 183, 1835–1842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Tu X., Latifi T., Bougdour A., Gottesman S., and Groisman E. A. (2006) The PhpP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. Proc. Natl. Acad. Sci. USA, 103, 13503–13508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Typas A., Barembruch C., Possling A., and Hengge R. (2007) Stationary phase reorganisation of the E. coli transcription machinery by Crl protein, a fine-tuner of σS activity and levels. EMBO J., 26, 1569–1578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Zhou Y., and Gottesman S. (2006) Modes of regulation of RpoS by H-NS. J. Bacteriol., 188, 7022–7025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Jishage M., Iwata A., Ueda S., and Ishihama A. (1996) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: Intracellular levels of four species of sigma subunit under various growth conditions. J. Bacteriol., 178, 5447–5451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Colland F., Fujita N., Ishihama A., and Kolb A. (2002) The interaction between σS, the stationary phase a factor, and the core enzyme of Escherichia coli RNA polymerase. Genes to Cells, 7, 233–247. [DOI] [PubMed] [Google Scholar]
  • 91.Maeda H., Fujita N., and Ishihama A. (2000) Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase. Nucl. Acids Res., 28, 3497–3503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Bernardo L., Johansson L., Solera D., Skarfstad E., and Shingler V. (2006) The guanosine tetraphosphate (ppGpp) alarmone, DksA and promoter affinity for RNA polymerase in regulation of sigma-dependent transcription. Mol. Microbiol., 60, 749–764. [DOI] [PubMed] [Google Scholar]
  • 93.Jishage M., Kvint K., Shingler V., and Nyström T. (2002) Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev., 16, 1260–1270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Ilag L. L. et al. (2004) Mass spectrometry of Escherichia coli RNA polymerase: interactions of the core enzyme with sigma70 and Rsd protein. Structure (Comb.), 12, 269–275. [DOI] [PubMed] [Google Scholar]
  • 95.Wassarman K. M., and Storz G. (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell, 101, 613–623. [DOI] [PubMed] [Google Scholar]
  • 96.Raffaelle M., Kanin E., Vogt J., Burgess R. R., and Ansari A. Z. (2005) Holoenzyme switching and stochastic release of sigma factors from RNA polymerase in vivo. Mol. Cell, 20, 357–366. [DOI] [PubMed] [Google Scholar]
  • 97.Gaal T. et al. (2001) Promoter recognition and discrimination by EσS RNA polymerase. Mol. Microbiol., 42, 939–954. [DOI] [PubMed] [Google Scholar]
  • 98.Typas A., and Hengge R. (2006) Role of the spacer between the −35 and–10 region in σS promoter selectivity in Escherichia coli. Mol. Microbiol., 59, 1037–1051. [DOI] [PubMed] [Google Scholar]
  • 99.Typas A., and Hengge R. (2005) Differential ability of σS and σ70 of Escherichia coli to utilize promoters containing half or full UP-element sites. Mol. Microbiol., 55, 250–260. [DOI] [PubMed] [Google Scholar]
  • 100.Colland F., Barth M., Hengge-Aronis R., and Kolb A. (2000) Sigma factor selectivity of Escherichia coli RNA polymerase: a role for CRP, IHF and Lrp transcription factors. EMBO J., 19, 3028–3037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Germer J., Becker G., Metzner M., and Hengge-Aronis R. (2001) Role of activator site position and a distal UP-element half-site for sigma factor selectivity at a CRP/H-NS activated σS-dependent promoter in Escherichia coli. Mol. Microbiol., 41, 705–716. [DOI] [PubMed] [Google Scholar]
  • 102.Bordes P. et al. (2003) DNA supercoiling contributes to disconnect σS accumulation from σS-dependent transcription in Escherichia coli. Mol. Microbiol., 48, 561–571. [DOI] [PubMed] [Google Scholar]
  • 103.Kusano S., Ding Q. Q., Fujita N., and Ishihama A. (1996) Promoter selectivity of Escherichia coli RNA polymerase Eσ70 and Eσ38 holoenzymes–Effect of DNA supercoiling. J. Biol. Chem., 271, 1998–2004. [DOI] [PubMed] [Google Scholar]
  • 104.Rosenthal A. Z., Hu M., and Gralla J. D. (2006) Osmolyte-induced transcription: −35 region elements and recognition by sigma38 (RpoS). Mol. Microbiol., 59, 1052–1061. [DOI] [PubMed] [Google Scholar]
  • 105.Gralla J. D., and Vargas D. R. (2006) Potassium glutamate as a transcriptional inhibitor during bacterial osmoregulation. EMBO J., 25, 1515–1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 106.Nonaka G., Blankschien M., Herman C., Gross C. A., and Rhodius V. A. (2006) Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. Genes Dev., 20, 1776–1789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 107.Rhodius V. A., Suh W. C., Nonaka G., West J., and Gross C. A. (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLOS biology, 4, e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 108.Wade J. et al. (2006) Extensive functional overlap between sigma factors in Escherichia coli. Nat. Struct. Mol. Biol., 13, 806–814. [DOI] [PubMed] [Google Scholar]
  • 109.Hengge-Aronis R. (2000) In: Storz G., and Hengge-Aronis R. (eds.), Bacterial Stress Responses, pp. 161–178 (ASM Press, Washington, D.C: ). [Google Scholar]
  • 110.Lange R., and Hengge-Aronis R. (1991) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol., 5, 49–59. [DOI] [PubMed] [Google Scholar]
  • 111.Loewen P. C., and Hengge-Aronis R. (1994) The role of the sigma factor σS (KatF) in bacterial global regulation. Annu. Rev. Microbiol., 48, 53–80. [DOI] [PubMed] [Google Scholar]
  • 112.Lacour S., and Landini P. (2004) σS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σS-dependent genes and identification of their promoter sequences. J. Bacteriol., 186, 7186–7195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 113.Patten C. L., Kirchhhof M. G., Schertzberg M. R., Morton R. A., and Schellhorn H. E. (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics, 272, 580–591. [DOI] [PubMed] [Google Scholar]
  • 114.Foster J. W. (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol., 2, 898–907. [DOI] [PubMed] [Google Scholar]
  • 115.Masuda N., and Church G. M. (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol. Microbiol., 48, 699–712. [DOI] [PubMed] [Google Scholar]
  • 116.Ma Z. et al. (2003) GadE(YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol. Microbiol., 49, 1309–1320. [DOI] [PubMed] [Google Scholar]
  • 117.Opdyke J. A., Kang J.-G., and Storz G. (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol., 186, 6698–6705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 118.Römling U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci., 62, 1234–1246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 119.Weber H., Pesavento C., Possling A., Tischendorf G., and Hengge R. (2006) Cyclic-di-GMP-mediated signaling within the σS network of Escherichia coli. Mol. Microbiol., 62, 1014–1034. [DOI] [PubMed] [Google Scholar]
  • 120.Jenal U. (2004) Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol., 7, 185–191. [DOI] [PubMed] [Google Scholar]
  • 121.Römling U., Gomelsky M., and Galperin M. Y. (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol., 57, 629–639. [DOI] [PubMed] [Google Scholar]
  • 122.Jenal U., and Malone J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet., 40, 385–407. [DOI] [PubMed] [Google Scholar]
  • 123.Ryjenkov D. A., Simm R., Römling U., and Gomelsky M. (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol Chem., 281, 30310–30314. [DOI] [PubMed] [Google Scholar]
  • 124.Amikam D., and Galperin M. Y. (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics, 22, 3–6. [DOI] [PubMed] [Google Scholar]
  • 125.Ko M., and Park C. (2000) H-NS-dependent regulation of flagellar synthesis is mediated by a LysR family protein. J. Bacteriol., 182, 4670–4672. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Science Progress are provided here courtesy of SAGE Publications

RESOURCES