Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1994 Jul;176(13):4104–4110. doi: 10.1128/jb.176.13.4104-4110.1994

The dacF-spoIIA operon of Bacillus subtilis, encoding sigma F, is autoregulated.

R Schuch 1, P J Piggot 1
PMCID: PMC205609  PMID: 8021191

Abstract

The spoIIA operon of Bacillus subtilis encodes sigma F and two proteins that may regulate sigma factor activity. High level induction of the tricistronic spoIIA operon occurs early during spore formation. At later times, the locus is cotranscribed with the upstream gene dacF, which encodes a putative DD-carboxypeptidase. In this study, the regulation of dacF-spoIIA transcription has been analyzed. Expression of a dacF-lacZ transcriptional fusion during sporulation required sigma F but not the later-expressed sporulation-associated sigma factors. Induction of sigma F synthesis during vegetative growth caused expression of dacF-lacZ fusions. The dacF-spoIIA promoter sequence is similar to sequences of previously identified sigma F promoters. It is concluded that dacF-spoIIA is transcribed by E sigma F. We present evidence that dacF-spoIIA is also transcribed by E sigma G, as is the case for the three other promoters known to be transcribed by E sigma F.

Full text

PDF
4104

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bylund J. E., Zhang L., Haines M. A., Higgins M. L., Piggot P. J. Analysis by fluorescence microscopy of the development of compartment-specific gene expression during sporulation of Bacillus subtilis. J Bacteriol. 1994 May;176(10):2898–2905. doi: 10.1128/jb.176.10.2898-2905.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Coote J. G. Sporulation in Bacillus subtilis. Genetic analysis of oligosporogenous mutants. J Gen Microbiol. 1972 Jun;71(1):17–27. doi: 10.1099/00221287-71-1-17. [DOI] [PubMed] [Google Scholar]
  3. Coppolecchia R., DeGrazia H., Moran C. P., Jr Deletion of spoIIAB blocks endospore formation in Bacillus subtilis at an early stage. J Bacteriol. 1991 Nov;173(21):6678–6685. doi: 10.1128/jb.173.21.6678-6685.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dubnau E., Weir J., Nair G., Carter L., 3rd, Moran C., Jr, Smith I. Bacillus sporulation gene spo0H codes for sigma 30 (sigma H). J Bacteriol. 1988 Mar;170(3):1054–1062. doi: 10.1128/jb.170.3.1054-1062.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Errington J. Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev. 1993 Mar;57(1):1–33. doi: 10.1128/mr.57.1.1-33.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fort P., Piggot P. J. Nucleotide sequence of sporulation locus spoIIA in Bacillus subtilis. J Gen Microbiol. 1984 Aug;130(8):2147–2153. doi: 10.1099/00221287-130-8-2147. [DOI] [PubMed] [Google Scholar]
  7. Gholamhoseinian A., Piggot P. J. Timing of spoII gene expression relative to septum formation during sporulation of Bacillus subtilis. J Bacteriol. 1989 Oct;171(10):5747–5749. doi: 10.1128/jb.171.10.5747-5749.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Henriques A. O., de Lencastre H., Piggot P. J. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie. 1992 Jul-Aug;74(7-8):735–748. doi: 10.1016/0300-9084(92)90146-6. [DOI] [PubMed] [Google Scholar]
  9. Hranueli D., Piggot P. J., Mandelstam J. Statistical estimate of the total number of operons specific for Bacillus subtilis sporulation. J Bacteriol. 1974 Sep;119(3):684–690. doi: 10.1128/jb.119.3.684-690.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ionesco H., Michel J., Cami B., Schaeffer P. Symposium on bacterial spores: II. Genetics of sporulation in Bacillus subtilis Marburg. J Appl Bacteriol. 1970 Mar;33(1):13–24. doi: 10.1111/j.1365-2672.1970.tb05230.x. [DOI] [PubMed] [Google Scholar]
  11. Itaya M., Kondo K., Tanaka T. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome. Nucleic Acids Res. 1989 Jun 12;17(11):4410–4410. doi: 10.1093/nar/17.11.4410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jonas R. M., Haldenwang W. G. Influence of spo mutations on sigma E synthesis in Bacillus subtilis. J Bacteriol. 1989 Sep;171(9):5226–5228. doi: 10.1128/jb.171.9.5226-5228.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Karmazyn-Campelli C., Bonamy C., Savelli B., Stragier P. Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis. Genes Dev. 1989 Feb;3(2):150–157. doi: 10.1101/gad.3.2.150. [DOI] [PubMed] [Google Scholar]
  14. Kroos L., Kunkel B., Losick R. Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science. 1989 Jan 27;243(4890):526–529. doi: 10.1126/science.2492118. [DOI] [PubMed] [Google Scholar]
  15. Kunkel B., Sandman K., Panzer S., Youngman P., Losick R. The promoter for a sporulation gene in the spoIVC locus of Bacillus subtilis and its use in studies of temporal and spatial control of gene expression. J Bacteriol. 1988 Aug;170(8):3513–3522. doi: 10.1128/jb.170.8.3513-3522.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Liu H. M., Chak K. F., Piggot P. J. Isolation and characterization of a recombinant plasmid carrying a functional part of the Bacillus subtilis spoIIA locus. J Gen Microbiol. 1982 Nov;128(11):2805–2812. doi: 10.1099/00221287-128-11-2805. [DOI] [PubMed] [Google Scholar]
  17. 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. doi: 10.1038/355601a0. [DOI] [PubMed] [Google Scholar]
  18. Losick R., Youngman P., Piggot P. J. Genetics of endospore formation in Bacillus subtilis. Annu Rev Genet. 1986;20:625–669. doi: 10.1146/annurev.ge.20.120186.003205. [DOI] [PubMed] [Google Scholar]
  19. 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. doi: 10.1126/science.1948031. [DOI] [PubMed] [Google Scholar]
  20. Miyao A., Theeragool G., Takeuchi M., Kobayashi Y. Bacillus subtilis spoVE gene is transcribed by sigma E-associated RNA polymerase. J Bacteriol. 1993 Jul;175(13):4081–4086. doi: 10.1128/jb.175.13.4081-4086.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nicholson W. L., Sun D. X., Setlow B., Setlow P. Promoter specificity of sigma G-containing RNA polymerase from sporulating cells of Bacillus subtilis: identification of a group of forespore-specific promoters. J Bacteriol. 1989 May;171(5):2708–2718. doi: 10.1128/jb.171.5.2708-2718.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Partridge S. R., Errington J. The importance of morphological events and intercellular interactions in the regulation of prespore-specific gene expression during sporulation in Bacillus subtilis. Mol Microbiol. 1993 May;8(5):945–955. doi: 10.1111/j.1365-2958.1993.tb01639.x. [DOI] [PubMed] [Google Scholar]
  23. Partridge S. R., Foulger D., Errington J. The role of sigma F in prespore-specific transcription in Bacillus subtilis. Mol Microbiol. 1991 Mar;5(3):757–767. doi: 10.1111/j.1365-2958.1991.tb00746.x. [DOI] [PubMed] [Google Scholar]
  24. Perego M., Wu J. J., Spiegelman G. B., Hoch J. A. Mutational dissociation of the positive and negative regulatory properties of the Spo0A sporulation transcription factor of Bacillus subtilis. Gene. 1991 Apr;100:207–212. doi: 10.1016/0378-1119(91)90368-l. [DOI] [PubMed] [Google Scholar]
  25. Piggot P. J., Chak K. F., Bugaichuk U. D. Isolation and characterization of a clone of the spoVE locus of Bacillus subtilis. J Gen Microbiol. 1986 Jul;132(7):1875–1881. doi: 10.1099/00221287-132-7-1875. [DOI] [PubMed] [Google Scholar]
  26. Piggot P. J., Coote J. G. Genetic aspects of bacterial endospore formation. Bacteriol Rev. 1976 Dec;40(4):908–962. doi: 10.1128/br.40.4.908-962.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Piggot P. J., Curtis C. A. Analysis of the regulation of gene expression during Bacillus subtilis sporulation by manipulation of the copy number of spo-lacZ fusions. J Bacteriol. 1987 Mar;169(3):1260–1266. doi: 10.1128/jb.169.3.1260-1266.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Piggot P. J., Curtis C. A., de Lencastre H. Use of integrational plasmid vectors to demonstrate the polycistronic nature of a transcriptional unit (spoIIA) required for sporulation of Bacillus subtilis. J Gen Microbiol. 1984 Aug;130(8):2123–2136. doi: 10.1099/00221287-130-8-2123. [DOI] [PubMed] [Google Scholar]
  29. Piggot P. J. Mapping of asporogenous mutations of Bacillus subtilis: a minimum estimate of the number of sporeulation operons. J Bacteriol. 1973 Jun;114(3):1241–1253. doi: 10.1128/jb.114.3.1241-1253.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sandman K., Kroos L., Cutting S., Youngman P., Losick R. Identification of the promoter for a spore coat protein gene in Bacillus subtilis and studies on the regulation of its induction at a late stage of sporulation. J Mol Biol. 1988 Apr 5;200(3):461–473. doi: 10.1016/0022-2836(88)90536-0. [DOI] [PubMed] [Google Scholar]
  31. Savva D., Mandelstam J. Synthesis of spoIIA and spoVA mRNA in Bacillus subtilis. J Gen Microbiol. 1986 Nov;132(11):3005–3011. doi: 10.1099/00221287-132-11-3005. [DOI] [PubMed] [Google Scholar]
  32. Schmidt R., Margolis P., Duncan L., Coppolecchia R., Moran C. P., 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. doi: 10.1073/pnas.87.23.9221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shimotsu H., Henner D. J. Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis. Gene. 1986;43(1-2):85–94. doi: 10.1016/0378-1119(86)90011-9. [DOI] [PubMed] [Google Scholar]
  34. Stragier P., Bonamy C., Karmazyn-Campelli C. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell. 1988 Mar 11;52(5):697–704. doi: 10.1016/0092-8674(88)90407-2. [DOI] [PubMed] [Google Scholar]
  35. Sun D. X., Cabrera-Martinez R. M., Setlow P. Control of transcription of the Bacillus subtilis spoIIIG gene, which codes for the forespore-specific transcription factor sigma G. J Bacteriol. 1991 May;173(9):2977–2984. doi: 10.1128/jb.173.9.2977-2984.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sun D. X., Stragier P., Setlow P. Identification of a new sigma-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. Genes Dev. 1989 Feb;3(2):141–149. doi: 10.1101/gad.3.2.141. [DOI] [PubMed] [Google Scholar]
  37. Sun D., Fajardo-Cavazos P., Sussman M. D., Tovar-Rojo F., Cabrera-Martinez R. M., Setlow P. Effect of chromosome location of Bacillus subtilis forespore genes on their spo gene dependence and transcription by E sigma F: identification of features of good E sigma F-dependent promoters. J Bacteriol. 1991 Dec;173(24):7867–7874. doi: 10.1128/jb.173.24.7867-7874.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sussman M. D., Setlow P. Cloning, nucleotide sequence, and regulation of the Bacillus subtilis gpr gene, which codes for the protease that initiates degradation of small, acid-soluble proteins during spore germination. J Bacteriol. 1991 Jan;173(1):291–300. doi: 10.1128/jb.173.1.291-300.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Trempy J. E., Bonamy C., Szulmajster J., Haldenwang W. G. Bacillus subtilis sigma factor sigma 29 is the product of the sporulation-essential gene spoIIG. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4189–4192. doi: 10.1073/pnas.82.12.4189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weir J., Predich M., Dubnau E., Nair G., Smith I. Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor. J Bacteriol. 1991 Jan;173(2):521–529. doi: 10.1128/jb.173.2.521-529.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wu J. J., Howard M. G., Piggot P. J. Regulation of transcription of the Bacillus subtilis spoIIA locus. J Bacteriol. 1989 Feb;171(2):692–698. doi: 10.1128/jb.171.2.692-698.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wu J. J., Piggot P. J., Tatti K. M., Moran C. P., Jr Transcription of the Bacillus subtilis spoIIA locus. Gene. 1991 May 15;101(1):113–116. doi: 10.1016/0378-1119(91)90231-y. [DOI] [PubMed] [Google Scholar]
  43. Wu J. J., Schuch R., Piggot P. J. Characterization of a Bacillus subtilis sporulation operon that includes genes for an RNA polymerase sigma factor and for a putative DD-carboxypeptidase. J Bacteriol. 1992 Aug;174(15):4885–4892. doi: 10.1128/jb.174.15.4885-4892.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yansura D. G., Henner D. J. Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. Proc Natl Acad Sci U S A. 1984 Jan;81(2):439–443. doi: 10.1073/pnas.81.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. de Lencastre H., Piggot P. J. Identification of different sites of expression for spo loci by transformation of Bacillus subtilis. J Gen Microbiol. 1979 Oct;114(2):377–389. doi: 10.1099/00221287-114-2-377. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES