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J Bacteriol. Jan 1995; 177(1): 123–133.
PMCID: PMC176564

Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor sigma B in response to environmental signals.

Abstract

sigma B of the gram-positive bacterium Bacillus subtilis is an alternative transcription factor activated by a variety of environmental stresses, including the stress imposed upon entry into the stationary growth phase. Previous reports have shown that this stationary-phase activation is enhanced when cells are grown in rich medium containing glucose and glutamine. The sigma B structural gene, sigB, lies in an operon with three other genes whose products have been shown to control sigma B activity in response to environmental stress. However, none of these is sufficient to explain the enhanced stationary-phase activation of sigma B in response to glucose. We show here that the four genes previously identified in the sigB operon constitute the downstream half of an eight-gene operon. The complete sigB operon is preceded by a sigma A-like promoter (PA) and has the order PA-orfR-orfS-orfT-orfU-PB-rsbV-rsbW-sig B-rsbX, where rsb stands for regulator of sigma-B and the previously identified sigma B-dependent promoter (PB) is an internal promoter preceding the downstream four-gene cluster. Although the genes downstream of PB were also transcribed by polymerase activity originating at PA, this transcription into the downstream cluster was not essential for normal induction of a sigma B-dependent ctc-lacZ fusion. However, deletion of all four upstream open reading frames was found to interfere with induction of the ctc-lacZ fusion in response to glucose. Additional deletion analysis and complementation studies showed that orfU was required for full glucose induction of sigma B-dependent genes. orfU encodes a trans-acting, positive factor with significant sequence identity to the RsbX negative regulator of sigma B. On the basis of these results, we rename orfU as rsbU to symbolize the regulatory role of its product.

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Selected References

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  • Alper S, Duncan L, Losick R. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell. 1994 Apr 22;77(2):195–205. [PubMed]
  • Benson AK, Haldenwang WG. Characterization of a regulatory network that controls sigma B expression in Bacillus subtilis. J Bacteriol. 1992 Feb;174(3):749–757. [PMC free article] [PubMed]
  • Benson AK, Haldenwang WG. Bacillus subtilis sigma B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2330–2334. [PMC free article] [PubMed]
  • Benson AK, Haldenwang WG. The sigma B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol. 1993 Apr;175(7):1929–1935. [PMC free article] [PubMed]
  • Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. [PMC free article] [PubMed]
  • Boylan SA, Redfield AR, Brody MS, Price CW. Stress-induced activation of the sigma B transcription factor of Bacillus subtilis. J Bacteriol. 1993 Dec;175(24):7931–7937. [PMC free article] [PubMed]
  • Boylan SA, Redfield AR, Price CW. Transcription factor sigma B of Bacillus subtilis controls a large stationary-phase regulon. J Bacteriol. 1993 Jul;175(13):3957–3963. [PMC free article] [PubMed]
  • Boylan SA, Rutherford A, Thomas SM, Price CW. Activation of Bacillus subtilis transcription factor sigma B by a regulatory pathway responsive to stationary-phase signals. J Bacteriol. 1992 Jun;174(11):3695–3706. [PMC free article] [PubMed]
  • Boylan SA, Thomas MD, Price CW. Genetic method to identify regulons controlled by nonessential elements: isolation of a gene dependent on alternate transcription factor sigma B of Bacillus subtilis. J Bacteriol. 1991 Dec;173(24):7856–7866. [PMC free article] [PubMed]
  • Dubnau D, Davidoff-Abelson R. Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex. J Mol Biol. 1971 Mar 14;56(2):209–221. [PubMed]
  • Dufour A, Haldenwang WG. Interactions between a Bacillus subtilis anti-sigma factor (RsbW) and its antagonist (RsbV). J Bacteriol. 1994 Apr;176(7):1813–1820. [PMC free article] [PubMed]
  • Duncan L, Losick R. SpoIIAB is an anti-sigma factor that binds to and inhibits transcription by regulatory protein sigma F from Bacillus subtilis. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2325–2329. [PMC free article] [PubMed]
  • Errington J. Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev. 1993 Mar;57(1):1–33. [PMC free article] [PubMed]
  • Ferrari FA, Ferrari E, Hoch JA. Chromosomal location of a Bacillus subtilis DNA fragment uniquely transcribed by sigma-28-containing RNA polymerase. J Bacteriol. 1982 Nov;152(2):780–785. [PMC free article] [PubMed]
  • Helmann JD, Chamberlin MJ. Structure and function of bacterial sigma factors. Annu Rev Biochem. 1988;57:839–872. [PubMed]
  • 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. [PubMed]
  • Hill KF, Mueller JP, Taber HW. The Bacillus subtilis menCD promoter is responsive to extracellular pH. Arch Microbiol. 1990;153(4):355–359. [PubMed]
  • Hoch JA. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu Rev Microbiol. 1993;47:441–465. [PubMed]
  • Holmes DS, Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. [PubMed]
  • Huisman GW, Kolter R. Sensing starvation: a homoserine lactone--dependent signaling pathway in Escherichia coli. Science. 1994 Jul 22;265(5171):537–539. [PubMed]
  • Igo M, Lampe M, Ray C, Schafer W, Moran CP, Jr, Losick R. Genetic studies of a secondary RNA polymerase sigma factor in Bacillus subtilis. J Bacteriol. 1987 Aug;169(8):3464–3469. [PMC free article] [PubMed]
  • Igo MM, Losick R. Regulation of a promoter that is utilized by minor forms of RNA polymerase holoenzyme in Bacillus subtilis. J Mol Biol. 1986 Oct 20;191(4):615–624. [PubMed]
  • Kaiser D, Losick R. How and why bacteria talk to each other. Cell. 1993 Jun 4;73(5):873–885. [PubMed]
  • Kalman S, Duncan ML, Thomas SM, Price CW. Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J Bacteriol. 1990 Oct;172(10):5575–5585. [PMC free article] [PubMed]
  • LeDeaux JR, Grossman AD. Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis. J Bacteriol. 1995 Jan;177(1):166–175. [PMC free article] [PubMed]
  • Losick R, Stragier P. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis. Nature. 1992 Feb 13;355(6361):601–604. [PubMed]
  • Magnuson R, Solomon J, Grossman AD. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell. 1994 Apr 22;77(2):207–216. [PubMed]
  • Margolis P, Driks A, Losick R. Establishment of cell type by compartmentalized activation of a transcription factor. Science. 1991 Oct 25;254(5031):562–565. [PubMed]
  • Matin A. The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):3–10. [PubMed]
  • Miller P, Mueller J, Hill K, Taber H. Transcriptional regulation of a promoter in the men gene cluster of Bacillus subtilis. J Bacteriol. 1988 Jun;170(6):2742–2748. [PMC free article] [PubMed]
  • Moran CP, Jr, Johnson WC, Losick R. Close contacts between sigma 37-RNA polymerase and a Bacillus subtilis chromosomal promoter. J Mol Biol. 1982 Dec 15;162(3):709–713. [PubMed]
  • Parkinson JS. Signal transduction schemes of bacteria. Cell. 1993 Jun 4;73(5):857–871. [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Price CW, Doi RH. Genetic mapping of rpoD implicates the major sigma factor of Bacillus subtilis RNA polymerase in sporulation initiation. Mol Gen Genet. 1985;201(1):88–95. [PubMed]
  • Schmidt R, Margolis P, Duncan L, Coppolecchia R, Moran CP, Jr, Losick R. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9221–9225. [PMC free article] [PubMed]
  • Siegele DA, Kolter R. Life after log. J Bacteriol. 1992 Jan;174(2):345–348. [PMC free article] [PubMed]
  • Straus DB, Walter WA, Gross CA. The heat shock response of E. coli is regulated by changes in the concentration of sigma 32. Nature. 1987 Sep 24;329(6137):348–351. [PubMed]
  • Varón D, Boylan SA, Okamoto K, Price CW. Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B. J Bacteriol. 1993 Jul;175(13):3964–3971. [PMC free article] [PubMed]
  • Voelker U, Dufour A, Haldenwang WG. The Bacillus subtilis rsbU gene product is necessary for RsbX-dependent regulation of sigma B. J Bacteriol. 1995 Jan;177(1):114–122. [PMC free article] [PubMed]
  • Völker U, Engelmann S, Maul B, Riethdorf S, Völker A, Schmid R, Mach H, Hecker M. Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology. 1994 Apr;140(Pt 4):741–752. [PubMed]

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