1887

Abstract

Extracytoplasmic function (ECF) sigma factors constitute a diverse family of proteins, within the class of the sigma 70 subunit of RNA polymerase. Most members of the family studied to date are known to regulate gene expression in response to stress conditions. The genome encodes at least 17 distinct sigma factors, seven of which are members of the ECF subfamily. Among these, five sigma factors, namely SigV, SigW, SigX, SigY and SigM, are encoded by the first genes of the cognate sigma operons. Disruption or repressed expression of the downstream gene(s) resulted in transcriptional activation of the cognate sigma operon. Moreover, protein–protein interaction analyses by yeast two-hybrid experiments indicated that these immediate downstream gene products bind the cognate ECF sigma factor, suggesting that they function as anti-sigma factors by capturing sigma factor on the inner surface of the cytoplasmic membrane. Interaction with other sigma factors was not observed. The results presented here also show that these anti-sigma factors interact with ECF sigma factors through their N-terminal region, implying that the N-terminal domain resides inside the cytoplasmic membrane.

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2004-03-01
2024-04-16
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References

  1. Asai K., Yamaguchi H., Kang C. M., Yoshida K., Fujita Y., Sadaie Y. 2003; DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220:155–160 [CrossRef]
    [Google Scholar]
  2. Bentley S. D., Chater K. F., Cerdeno-Tarraga A. M.40 other authors 2002; Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147 [CrossRef]
    [Google Scholar]
  3. Braun V. 1997; Surface signaling: novel transcription initiation mechanism starting from the cell surface. Arch Microbiol 167:325–331 [CrossRef]
    [Google Scholar]
  4. Browning D. F., Whitworth D. E., Hodgson D. A. 2003; Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol Microbiol 48:237–251 [CrossRef]
    [Google Scholar]
  5. Brutsche S., Braun V. 1997; SigX of Bacillus subtilis replaces the ECF sigma factor FecI of Escherichia coli and is inhibited by RsiX. Mol Gen Genet 256:416–425 [CrossRef]
    [Google Scholar]
  6. Campbell E. A., Tupy J. L., Gruber T. M., Wang S., Sharp M. M., Gross C. A., Darst S. A. 2003; Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol Cell 11:1067–1078 [CrossRef]
    [Google Scholar]
  7. Cao M., Salzberg L., Tsai C. S., Mascher T., Bonilla C., Wang T., Ye R. W., Marquez-Magana L., Helmann J. D. 2003; Regulation of the Bacillus subtilis extracytoplasmic function protein sigma(Y) and its target promoters. J Bacteriol 185:4883–4890 [CrossRef]
    [Google Scholar]
  8. Cole S. T., Brosch R., Parkhill J.39 other authors 1998; Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544 [CrossRef]
    [Google Scholar]
  9. De Las Penas A., Connolly L., Gross C. A. 1997; The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol Microbiol 24:373–385 [CrossRef]
    [Google Scholar]
  10. Enz S., Mahren S., Stroeher U. H., Braun V. 2000; Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J Bacteriol 182:637–646 [CrossRef]
    [Google Scholar]
  11. Fukuchi K., Kasahara Y., Asai K., Kobayashi K., Moriya S., Ogasawara N. 2000; The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology 146:1573–1583
    [Google Scholar]
  12. Gietz R. D., Schiestl R. H. 1995; Transforming yeast with DNA. Methods Mol Cell Biol 5:255–269
    [Google Scholar]
  13. Gorham H. C., McGowan S. J., Robson P. R., Hodgson D. A. 1996; Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol Microbiol 19:171–186 [CrossRef]
    [Google Scholar]
  14. Helmann J. D. 2002; The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110
    [Google Scholar]
  15. Hershberger C. D., Ye R. W., Parsek M. R., Xie Z. D., Chakrabarty A. M. 1995; The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E). Proc Natl Acad Sci U S A 92:7941–7945 [CrossRef]
    [Google Scholar]
  16. Horsburgh M. J., Moir A. 1999; Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol 32:41–50 [CrossRef]
    [Google Scholar]
  17. Huang X., Decatur A., Sorokin A., Helmann J. D. 1997; The Bacillus subtilis sigma(X) protein is an extracytoplasmic function sigma factor contributing to survival at high temperature. J Bacteriol 179:2915–2921
    [Google Scholar]
  18. Huang X., Fredrick K. L., Helmann J. D. 1998; Promoter recognition by Bacillus subtilis sigmaW: autoregulation and partial overlap with the sigmaX regulon. J Bacteriol 180:3765–3770
    [Google Scholar]
  19. Ito T., Tashiro K., Muta S., Ozawa R., Chiba T., Nishizawa M., Yamamoto K., Kuhara S., Sakaki Y. 2000; Toward a protein-protein interaction map of the budding yeast: a comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc Natl Acad Sci U S A 97:1143–1147 [CrossRef]
    [Google Scholar]
  20. James P., Halladay J., Craig E. A. 1996; Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425–1436
    [Google Scholar]
  21. Kaneko T., Nakamura Y., Sato S.21 other authors 2000; Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338 [CrossRef]
    [Google Scholar]
  22. Kang J. G., Paget M. S., Seok Y. J., Hahn M. Y., Bae J. B., Hahn J. S., Kleanthous C., Buttner M. J., Roe J. H. 1999; RsrA, an anti-sigma factor regulated by redox change. EMBO J 18:4292–4298 [CrossRef]
    [Google Scholar]
  23. Kunst F., Ogasawara N., Moszer I.148 other authors 1997; The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256 [CrossRef]
    [Google Scholar]
  24. Li W., Stevenson C. E., Burton N., Jakimowicz P., Paget M. S., Buttner M. J., Lawson D. M., Kleanthous C. 2002; Identification and structure of the anti-sigma factor-binding domain of the disulphide-stress regulated sigma factor sigma(R) from Streptomyces coelicolor. J Mol Biol 323:225–236 [CrossRef]
    [Google Scholar]
  25. Liu H., Haga K., Yasumoto K., Ohashi Y., Yoshikawa H., Takahashi H. 1997; Sequence and analysis of a 31 kb segment of the Bacillus subtilis chromosome in the area of therrnH and rrnG operons. Microbiology 143:2763–2767 [CrossRef]
    [Google Scholar]
  26. Lonetto M. A., Brown K. L., Rudd K. E., Buttner M. J. 1994; Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A 91:7573–7577 [CrossRef]
    [Google Scholar]
  27. Mogk A., Homuth G., Scholz C., Kim L., Schmid F. X., Schumann W. 1997; The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J 16:4579–4590 [CrossRef]
    [Google Scholar]
  28. Moriya S., Tsujikawa E., Hassan A. K., Asai K., Kodama T., Ogasawara N. 1998; A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 29:179–187 [CrossRef]
    [Google Scholar]
  29. Newman J. D., Anthony J. R., Donohue T. J. 2001; The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor. J Mol Biol 313:485–499 [CrossRef]
    [Google Scholar]
  30. Ochsner U. A., Johnson Z., Lamont I. L., Cunliffe H. E., Vasil M. L. 1996; Exotoxin A production in Pseudomonas aeruginosa requires the iron-regulated pvdS gene encoding an alternative sigma factor. Mol Microbiol 21:1019–1028 [CrossRef]
    [Google Scholar]
  31. Paget M. S., Kang J. G., Roe J. H., Buttner M. J. 1998; sigmaR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17:5776–5782 [CrossRef]
    [Google Scholar]
  32. Paget M. S., Bae J. B., Hahn M. Y., Li W., Kleanthous C., Roe J. H., Buttner M. J. 2001; Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol Microbiol 39:1036–1047 [CrossRef]
    [Google Scholar]
  33. Raivio T. L., Silhavy T. J. 2001; Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55:591–624 [CrossRef]
    [Google Scholar]
  34. Rowen D. W., Deretic V. 2000; Membrane-to-cytosol redistribution of ECF sigma factor AlgU and conversion to mucoidy in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Mol Microbiol 36:314–327 [CrossRef]
    [Google Scholar]
  35. Sorokin A., Zumstein E., Azevedo V., Ehrlich S. D., Serror P. 1993; The organization of the Bacillus subtilis 168 chromosome region between the spoVA and serA genetic loci, based on sequence data. Mol Microbiol 10:385–395 [CrossRef]
    [Google Scholar]
  36. Sorokin A., Bolotin A., Purnelle B., Hilbert H., Lauber J., Dusterhoft A., Ehrlich S. D. 1997; Sequence of the Bacillus subtilis genome region in the vicinity of the lev operon reveals two new extracytoplasmic function RNA polymerase sigma factors SigV and SigZ. Microbiology 143:2939–2943 [CrossRef]
    [Google Scholar]
  37. Tojo S., Matsunaga M., Matsumoto T., Kang C. M., Yamaguchi H., Asai K., Sadaie Y., Yoshida K., Fujita Y. 2003; Organization and expression of the Bacillus subtilis sigY operon. J Biochem (Tokyo 134:935–946 [CrossRef]
    [Google Scholar]
  38. Vagner V., Dervyn E., Ehrlich S. D. 1998; A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144:3097–3104 [CrossRef]
    [Google Scholar]
  39. Yoshida K., Shindo K., Sano H., Seki S., Fujimura M., Yanai N., Miwa Y., Fujita Y. 1996; Sequencing of a 65 kb region of the Bacillus subtilis genome containing thelic and cel loci, and creation of a 177 kb contig covering the gnt–sacXY region. Microbiology 142:3113–3123 [CrossRef]
    [Google Scholar]
  40. Youngman P., Perkins J., Sandman K. 1985; Use of Tn917-mediated transcriptional gene fusions to lacZ and cat-86 for the identification and study of regulated genes in the Bacillus subtilis chromosome. In Molecular Biology of Microbial Differentiation pp 47–54 Edited by Hoch J. A., Setlow P. Washington, DC: American Society for Microbiology;
    [Google Scholar]
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