1887

Abstract

The regulon is induced by different stresses that most probably affect integrity of the cell envelope. The activity of the extracytoplasmic function (ECF) sigma factor is modulated by the transmembrane anti-sigma factor RsiW, which undergoes stress-induced degradation in a process known as regulated intramembrane proteolysis, finally resulting in the release of and the transcription of -controlled genes. Mutations in the gene, which encodes an ATP binding cassette (ABC) of an ABC transporter of unknown function, block site-2 proteolysis of RsiW by the intramembrane cleaving protease RasP (YluC). In addition, degradation of the cell division protein FtsL, which represents a second RasP substrate, is blocked in an -negative strain. The defect in induction of an -knockout strain could be partly suppressed by overproducing RasP. A -knockout strain displayed the same pleiotropic phenotype as an knockout, namely defects in processing -amylase, in competence development, and in formation of multicellular structures known as biofilms.

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2008-07-01
2020-07-15
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References

  1. Ades S. E.. 2004; Control of the alternative sigma factor σE in Escherichia coli. Curr Opin Microbiol7:157–162
    [Google Scholar]
  2. Akiyama Y., Kanehara K., Ito K.. 2004; RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. EMBO J23:4434–4442
    [Google Scholar]
  3. Alba B. M., Gross C. A.. 2004; Regulation of the Escherichia coli σE-dependent envelope stress response. Mol Microbiol52:613–619
    [Google Scholar]
  4. Bolhuis A., Matzen A., Hyyrylainen H. L., Kontinen V. P., Meima R., Chapuis J., Venema G., Bron S., Freudl R., Van Dijl J. M.. 1999; Signal peptide peptidase- and ClpP-like proteins of Bacillus subtilis required for efficient translocation and processing of secretory proteins. J Biol Chem274:24585–24592
    [Google Scholar]
  5. Bramkamp M., Weston L., Daniel R. A., Errington J.. 2006; Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis. Mol Microbiol62:580–591
    [Google Scholar]
  6. Branda S. S., Gonzalez-Pastor J. E., Ben-Yehuda S., Losick R., Kolter R.. 2001; Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A98:11621–11626
    [Google Scholar]
  7. Branda S. S., Gonzalez-Pastor J. E., Dervyn E., Ehrlich S. D., Losick R., Kolter R.. 2004; Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol186:3970–3979
    [Google Scholar]
  8. Butcher B. G., Helmann J. D.. 2006; Identification of Bacillus subtilis σW-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol60:765–782
    [Google Scholar]
  9. Cao M., Wang T., Ye R., Helmann J. D.. 2002; Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis σW and σM regulons. Mol Microbiol45:1267–1276
    [Google Scholar]
  10. Davidson A. L., Chen J.. 2004; ATP-binding cassette transporters in bacteria. Annu Rev Biochem73:241–268
    [Google Scholar]
  11. Deuerling E., Mogk A., Richter C., Purucker M., Schumann W.. 1997; The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol23:921–933
    [Google Scholar]
  12. Ellermeier C. D., Losick R.. 2006; Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev20:1911–1922
    [Google Scholar]
  13. Flynn J. M., Levchenko I., Sauer R. T., Baker T. A.. 2004; Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev18:2292–2301
    [Google Scholar]
  14. Grant S. G., Jessee J., Bloom F. R., Hanahan D.. 1990; Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A87:4645–4649
    [Google Scholar]
  15. Härtl B., Wehrl W., Wiegert T., Homuth G., Schumann W.. 2001; Development of a new integration site within the Bacillus subtilis chromosome and construction of compatible expression cassettes. J Bacteriol183:2696–2699
    [Google Scholar]
  16. Heinrich J., Wiegert T.. 2006; YpdC determines site-1 degradation in regulated intramembrane proteolysis of the RsiW anti-sigma factor of Bacillus subtilis. Mol Microbiol62:566–579
    [Google Scholar]
  17. Helmann J. D.. 2002; The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol46:47–110
    [Google Scholar]
  18. Helmann J. D.. 2006; Deciphering a complex genetic regulatory network: the Bacillus subtilis σW protein and intrinsic resistance to antimicrobial compounds. Sci Prog89:243–266
    [Google Scholar]
  19. Homuth G., Heinemann M., Zuber U., Schumann W.. 1996; The genes of lepA and hemN form a bicistronic operon in Bacillus subtilis. Microbiology142:1641–1649
    [Google Scholar]
  20. Homuth G., Masuda S., Mogk A., Kobayashi Y., Schumann W.. 1997; The dnaK operon of Bacillus subtilis is heptacistronic. J Bacteriol179:1153–1164
    [Google Scholar]
  21. Huang X., Fredrick K. L., Helmann J. D.. 1998; Promoter recognition by Bacillus subtilis σW: autoregulation and partial overlap with the σX regulon. J Bacteriol180:3765–3770
    [Google Scholar]
  22. Huang X., Gaballa A., Cao M., Helmann J. D.. 1999; Identification of target promoters for the Bacillus subtilis extracytoplasmic function σ factor σW. Mol Microbiol31:361–371
    [Google Scholar]
  23. Kearns D. B., Losick R.. 2003; Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol49:581–590
    [Google Scholar]
  24. Kim L., Mogk A., Schumann W.. 1996; A xylose inducible Bacillus subtilis integration vector and its application. Gene181:71–76
    [Google Scholar]
  25. Kobayashi K.. 2007; Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol189:4920–4931
    [Google Scholar]
  26. Kontinen V. P., Sarvas M.. 1988; Mutants of Bacillus subtilis defective in protein export. J Gen Microbiol134:2333–2344
    [Google Scholar]
  27. Leskela S., Kontinen V. P., Sarvas M.. 1996; Molecular analysis of an operon in Bacillus subtilis encoding a novel ABC transporter with a role in exoprotein production, sporulation and competence. Microbiology142:71–77
    [Google Scholar]
  28. Leskela S., Wahlstrom E., Hyyrylainen H. L., Jacobs M., Palva A., Sarvas M., Kontinen V. P.. 1999; Ecs, an ABC transporter of Bacillus subtilis: dual signal transduction functions affecting expression of secreted proteins as well as their secretion. Mol Microbiol31:533–543
    [Google Scholar]
  29. Makinoshima H., Glickman M. S.. 2005; Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature436:406–409
    [Google Scholar]
  30. Makinoshima H., Glickman M. S.. 2006; Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis. Microbes Infect8:1882–1888
    [Google Scholar]
  31. Mascher T., Hachmann A. B., Helmann J. D.. 2007; Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function σ factors. J Bacteriol189:6919–6927
    [Google Scholar]
  32. Nicholson W. L., Setlow P.. 1990; Sporulation, germination and outgrowth. . In Molecular Biological Methods for Bacillus pp391–450 Edited by Harwood C. R., Cutting S. M. Chichester, UK: Wiley;
  33. Otto M., Götz F. 2001; ABC transporters of staphylococci. Res Microbiol152:351–356
    [Google Scholar]
  34. Pietiäinen M., Gardemeister M., Mecklin M., Leskela S., Sarvas M., Kontinen V. P.. 2005; Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology151:1577–1592
    [Google Scholar]
  35. Pummi T., Leskela S., Wahlstrom E., Gerth U., Tjalsma H., Hecker M., Sarvas M., Kontinen V. P.. 2002; ClpXP protease regulates the signal peptide cleavage of secretory preproteins in Bacillus subtilis with a mechanism distinct from that of the Ecs ABC transporter. J Bacteriol184:1010–1018
    [Google Scholar]
  36. Quentin Y., Fichant G., Denizot F.. 1999; Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. J Mol Biol287:467–484
    [Google Scholar]
  37. Saito H., Shibata T., Ando T.. 1979; Mapping of genes determining nonpermissiveness and host-specific restriction to bacteriophages in Bacillus subtilis Marburg. Mol Gen Genet170:117–122
    [Google Scholar]
  38. Sambrook J., Russell D. W.. 2005; Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
  39. Schöbel S., Zellmeier S., Schumann W., Wiegert T.. 2004; The Bacillus subtilis σW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol Microbiol52:1091–1105
    [Google Scholar]
  40. Schumann W., Ehrlich S. D.. Ogasawara N.. (editors) 2001; Functional Analysis of Bacterial Genes: a Practical Manual Chichester, UK: Wiley;
    [Google Scholar]
  41. Stein T., Heinzmann S., Dusterhus S., Borchert S., Entian K. D.. 2005; Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. J Bacteriol187:822–828
    [Google Scholar]
  42. Suzuki T., Itoh A., Ichihara S., Mizushima S.. 1987; Characterization of the sppA gene coding for protease IV, a signal peptide peptidase of Escherichia coli. J Bacteriol169:2523–2528
    [Google Scholar]
  43. Weihofen A., Martoglio B.. 2003; Intramembrane-cleaving proteases: controlled liberation of proteins and bioactive peptides. Trends Cell Biol13:71–78
    [Google Scholar]
  44. Wickner W., Moore K., Dibb N., Geissert D., Rice M.. 1987; Inhibition of purified Escherichia coli leader peptidase by the leader (signal) peptide of bacteriophage M13 procoat. J Bacteriol169:3821–3822
    [Google Scholar]
  45. Wiegert T., Homuth G., Versteeg S., Schumann W.. 2001; Alkaline shock induces the Bacillus subtilis σW regulon. Mol Microbiol41:59–71
    [Google Scholar]
  46. Zellmeier S., Schumann W., Wiegert T.. 2006; Involvement of Clp protease activity in modulating the Bacillus subtilis σW stress response. Mol Microbiol61:1569–1582
    [Google Scholar]
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