1887

Abstract

The RNA polymerase core associated with transcribes many genes related to stress or to the stationary phase. When cells enter a phase of phosphate starvation, the transcription of several genes and operons, collectively known as the PHO regulon, is strongly induced. The promoters of the PHO genes hitherto analysed are recognized by -associated RNA polymerase. A mutation in the gene that encodes , , significantly increases the level of alkaline phosphatase activity and the overproduction of inhibits it. Other PHO genes such as and are likewise affected by . In contrast, , which encodes a periplasmic phosphate-binding protein and is a negative regulator of PHO, is stimulated by . The effect of on the PHO genes is at the transcriptional level. It is shown that a cytosine residue at position −13 is important for the positive effect of on . The interpretation of these observations is based on the competition between and for the binding to the core RNA polymerase.

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2004-09-01
2024-03-29
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References

  1. Aguena M., Yagil E., Spira B. 2002; Transcriptional analysis of the pst operon of Escherichia coli. Mol Genet Genomics 268:518–524 [CrossRef]
    [Google Scholar]
  2. Barik S. K., Prurshothaman C. S., Mohanty A. N. 2001; Phosphatase activity with reference to bacteria and phosphorus in tropical freshwater aquaculture pond systems. Aquac Res 32:819–832 [CrossRef]
    [Google Scholar]
  3. Becker G., 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 [CrossRef]
    [Google Scholar]
  4. Bordes P., Repoila F., Kolb A., Gutierrez C. 2000; Involvement of differential efficiency of transcription by EσS and Eσ70 RNA polymerase holoenzymes in growth phase regulation of theEscherichia coli osmE promoter. Mol Microbiol 35:845–853 [CrossRef]
    [Google Scholar]
  5. Bradford M. M. 1976; A rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  6. Chomczynski P., Sacchi N. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159
    [Google Scholar]
  7. Colland F., Barth M., Hengge-Aronis R., Kolb A. 2000; σ factor selectivity of Escherichia coli RNA polymerase: role for CRP, IHF and lrp transcription factors. EMBO J 19:3028–3037 [CrossRef]
    [Google Scholar]
  8. Dove S. L., Smith S. G., Dorman C. J. 1997; Control of Escherichia coli type 1 fimbrial gene expression in stationary phase: a negative role for RpoS. Mol Gen Genet 254:13–20 [CrossRef]
    [Google Scholar]
  9. Dykxhoorn D. M., St Pierre R., Linn T. 1996; A set of compatible tac promoter expression vectors. Gene 177:133–136 [CrossRef]
    [Google Scholar]
  10. Echols H., Garen A., Garen S., Torriani A. 1961; Genetic control of repression of alkaline phosphatase in E. coli. J Mol Biol 3:425–438 [CrossRef]
    [Google Scholar]
  11. Espinosa-Urgel M., Chamizo C., Tormo A. 1996; A consensus structure for σS-dependent promoters. Mol Microbiol 21:657–659 [CrossRef]
    [Google Scholar]
  12. Farewell A., Kvint K., Nyström T. 1998; Negative regulation by RpoS: a case of sigma factor competition. Mol Microbiol 29:1039–1051 [CrossRef]
    [Google Scholar]
  13. Gaal T., Ross W., Estrem S. T., Nguyen L. H., Burgess R. R., Gourse R. L. 2001; Promoter recognition and discrimination by EσS RNA polymerase. Mol Microbiol 42:939–954 [CrossRef]
    [Google Scholar]
  14. Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., Cashel M. 1993; Synthesis of the stationary-phase sigma factor σS is positively regulated by ppGpp. J Bacteriol 175:7982–7989
    [Google Scholar]
  15. Hengge-Aronis R. 1993; Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 72:165–168 [CrossRef]
    [Google Scholar]
  16. Hengge-Aronis R. 2000; The general stress response in Escherichia coli. In Bacterial Stress Responses pp. 161–178 Edited by Storz G., Hengge-Aronis R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  17. Hengge-Aronis R. 2002a; Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395 [CrossRef]
    [Google Scholar]
  18. Hengge-Aronis R. 2002b; Stationary phase gene regulation: what makes an Escherichia coli promoter σS-selective?. Curr Opin Microbiol 5:591–595 [CrossRef]
    [Google Scholar]
  19. Kusano S., Ding Q., Fujita N., Ishihama A. 1996; Promoter selectivity of Escherichia coli RNA polymerase Eσ70 and Eσ38 holoenzymes. Effect of DNA supercoiling. J Biol Chem 271:1998–2004 [CrossRef]
    [Google Scholar]
  20. Kvint K., Farewell A., Nyström T. 2000; RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of σS. J Biol Chem 275:14795–14798 [CrossRef]
    [Google Scholar]
  21. Lacour S., Kolb A., Landini P. 2003; Nucleotides from −16 to −12 determine specific promoter recognition by bacterial σS-RNA polymerase. J Biol Chem 278:37160–37168 [CrossRef]
    [Google Scholar]
  22. Lange R., Hengge-Aronis R. 1991; Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5:49–59 [CrossRef]
    [Google Scholar]
  23. Lee S. J., Gralla J. D. 2001; Sigma38 (rpoS) RNA polymerase promoter engagement via −10 region nucleotides. J Biol Chem 276:30064–30071 [CrossRef]
    [Google Scholar]
  24. Levinthal C., Signer E. R., Fetherolf K. 1962; Reactivation and hybridization of reduced alkaline phosphatase. Proc Natl Acad Sci U S A 48:1230–1237 [CrossRef]
    [Google Scholar]
  25. Makino K., Amemura M., Kim S. K., Nakata A., Shinagawa H. 1993; Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Genes Dev 7:149–160 [CrossRef]
    [Google Scholar]
  26. Makino K., Amemura M., Kawamoto T., Kimura S., Shinagawa H., Nakata A., Suzuki M. 1996; DNA binding of PhoB and its interaction with RNA polymerase. J Mol Biol 259:15–26 [CrossRef]
    [Google Scholar]
  27. Miller J. H. 1992 A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  28. Nguyen L. H., Jensen D. B., Thompson N. E., Gentry D. R., Burgess R. R. 1993; In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product. Biochemistry 32:11112–11117 [CrossRef]
    [Google Scholar]
  29. Notley-McRobb L., King T., Ferenci T. 2002; rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol 184:806–811 [CrossRef]
    [Google Scholar]
  30. Nyström T. 2003; Conditional senescence in bacteria: death of the immortals. Mol Microbiol 48:17–23 [CrossRef]
    [Google Scholar]
  31. Pratt L. A., Hsing W., Gibson K. E., Silhavy T. J. 1996; From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins inEscherichia coli. Mol Microbiol 20:911–917 [CrossRef]
    [Google Scholar]
  32. Ruiz N., Silhavy T. J. 2003; Constitutive activation of the Escherichia coli Pho regulon upregulates rpoS translation in an Hfq-dependent fashion. J Bacteriol 185:5984–5992 [CrossRef]
    [Google Scholar]
  33. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Schellhorn H. E., Audia J. P., Wei L. I., Chang L. 1998; Identification of conserved, RpoS-dependent stationary-phase genes of Escherichia coli. J Bacteriol 180:6283–6291
    [Google Scholar]
  35. Shaw W. V. 1975; Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria. Methods Enzymol 43:737–755
    [Google Scholar]
  36. Spira B., Yagil E. 1999; The integration host factor (IHF) affects the expression of the phosphate-binding protein and of alkaline phosphatase in Escherichia coli. Curr Microbiol 38:80–85 [CrossRef]
    [Google Scholar]
  37. Spira B., Silberstein N., Yagil E. 1995; Guanosine 3′,5′-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J Bacteriol 177:4053–4058
    [Google Scholar]
  38. Steed P. M., Wanner B. L. 1993; Use of the rep technique for allele replacement to construct mutants with deletions of the pstSCAB-phoU operon: evidence of a new role for the PhoU protein in the phosphate regulon. J Bacteriol 175:6797–6809
    [Google Scholar]
  39. Sundareshwar P. V., Morris J. T., Koepfler E. K., Fornwalt B. 2003; Phosphorus limitation of coastal ecosystem processes. Science 299:563–565 [CrossRef]
    [Google Scholar]
  40. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. 1993; Heterogeneity of the principal σfactor in Escherichia coli: the rpoS gene product, σ38, is a second principal σ factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A 90:3511–3515 [CrossRef]
    [Google Scholar]
  41. Torriani A. 1960; Influence of inorganic phosphates in the formation of phosphatases of Escherichia coli. Biochim Biophys Acta 38:460–469 [CrossRef]
    [Google Scholar]
  42. Wanner B. 1996; Phosphorus assimilation and control of the phosphate regulon. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp. 1357–1381 Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  43. Wise A., Brems R., Ramakrishnan V., Villarejo M. 1996; Sequences in the −35 region of Escherichia coli rpoS-dependent genes promote transcription by EσS. J Bacteriol 178:2785–2793
    [Google Scholar]
  44. Xu J., Johnson R. C. 1995; Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol 177:938–947
    [Google Scholar]
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