Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1992 May;174(10):3185–3195. doi: 10.1128/jb.174.10.3185-3195.1992

Interactions among mutations that cause altered timing of gene expression during sporulation in Bacillus subtilis.

K Ireton 1, A D Grossman 1
PMCID: PMC205985  PMID: 1315731

Abstract

The ski4::Tn917lac insertion mutation in Bacillus subtilis was isolated in a screen for mutations that cause a defect in sporulation but that are suppressed by the presence or overexpression of the histidine protein kinase encoded by kinA (spoIIJ). ski4::Tn917lac caused a small defect in sporulation, but in combination with a null mutation in kinA, it caused a much more severe defect. The insertion mutation was in an 87-amino-acid open reading frame (orf87 bofA) that controls the activation of a sigma factor, sigma K, at intermediate times during sporulation. The ski4 mutation caused the premature expression of cotA, a gene controlled by sigma K. An independent mutation that causes the premature activation of sigma K also caused a synthetic (synergistic) sporulation phenotype in combination with a null mutation in kinA, indicating that the defect was due to altered timing of gene expression directed by sigma K. Expression of ski4 was shown to be controlled by the sporulation-specific sigma factor sigma E.

Full text

PDF
3187

Images in this article

3190Image
on p.3190

Selected References

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

  1. Albright L. M., Huala E., Ausubel F. M. Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu Rev Genet. 1989;23:311–336. doi: 10.1146/annurev.ge.23.120189.001523. [DOI] [PubMed] [Google Scholar]
  2. Alonso J. C., Shirahige K., Ogasawara N. Molecular cloning, genetic characterization and DNA sequence analysis of the recM region of Bacillus subtilis. Nucleic Acids Res. 1990 Dec 11;18(23):6771–6777. doi: 10.1093/nar/18.23.6771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Antoniewski C., Savelli B., Stragier P. The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes. J Bacteriol. 1990 Jan;172(1):86–93. doi: 10.1128/jb.172.1.86-93.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boylan S. A., Chun K. T., Edson B. A., Price C. W. Early-blocked sporulation mutations alter expression of enzymes under carbon control in Bacillus subtilis. Mol Gen Genet. 1988 May;212(2):271–280. doi: 10.1007/BF00334696. [DOI] [PubMed] [Google Scholar]
  5. Boylan S. A., Thomas M. D., Price C. W. 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. doi: 10.1128/jb.173.24.7856-7866.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burbulys D., Trach K. A., Hoch J. A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell. 1991 Feb 8;64(3):545–552. doi: 10.1016/0092-8674(91)90238-t. [DOI] [PubMed] [Google Scholar]
  7. Chesnut R. S., Bookstein C., Hulett F. M. Separate promoters direct expression of phoAIII, a member of the Bacillus subtilis alkaline phosphatase multigene family, during phosphate starvation and sporulation. Mol Microbiol. 1991 Sep;5(9):2181–2190. doi: 10.1111/j.1365-2958.1991.tb02148.x. [DOI] [PubMed] [Google Scholar]
  8. Clarke S., Lopez-Diaz I., Mandelstam J. Use of lacZ gene fusions to determine the dependence pattern of the sporulation gene spoIID in spo mutants of Bacillus subtilis. J Gen Microbiol. 1986 Nov;132(11):2987–2994. doi: 10.1099/00221287-132-11-2987. [DOI] [PubMed] [Google Scholar]
  9. Cutting S., Oke V., Driks A., Losick R., Lu S., Kroos L. A forespore checkpoint for mother cell gene expression during development in B. subtilis. Cell. 1990 Jul 27;62(2):239–250. doi: 10.1016/0092-8674(90)90362-i. [DOI] [PubMed] [Google Scholar]
  10. Cutting S., Roels S., Losick R. Sporulation operon spoIVF and the characterization of mutations that uncouple mother-cell from forespore gene expression in Bacillus subtilis. J Mol Biol. 1991 Oct 20;221(4):1237–1256. doi: 10.1016/0022-2836(91)90931-u. [DOI] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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. doi: 10.1016/0022-2836(71)90460-8. [DOI] [PubMed] [Google Scholar]
  13. Errington J., Wootten L., Dunkerley J. C., Foulger D. Differential gene expression during sporulation in Bacillus subtilis: regulation of the spoVJ gene. Mol Microbiol. 1989 Aug;3(8):1053–1060. doi: 10.1111/j.1365-2958.1989.tb00255.x. [DOI] [PubMed] [Google Scholar]
  14. Ferrari F. A., Nguyen A., Lang D., Hoch J. A. Construction and properties of an integrable plasmid for Bacillus subtilis. J Bacteriol. 1983 Jun;154(3):1513–1515. doi: 10.1128/jb.154.3.1513-1515.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ferrari F. A., Trach K., LeCoq D., Spence J., Ferrari E., Hoch J. A. Characterization of the spo0A locus and its deduced product. Proc Natl Acad Sci U S A. 1985 May;82(9):2647–2651. doi: 10.1073/pnas.82.9.2647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Foulger D., Errington J. Sequential activation of dual promoters by different sigma factors maintains spoVJ expression during successive developmental stages of Bacillus subtilis. Mol Microbiol. 1991 Jun;5(6):1363–1373. doi: 10.1111/j.1365-2958.1991.tb00783.x. [DOI] [PubMed] [Google Scholar]
  17. Hahn J., Albano M., Dubnau D. Isolation and characterization of Tn917lac-generated competence mutants of Bacillus subtilis. J Bacteriol. 1987 Jul;169(7):3104–3109. doi: 10.1128/jb.169.7.3104-3109.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hay R. E., Tatti K. M., Vold B. S., Green C. J., Moran C. P., Jr Promoter used by sigma-29 RNA polymerase from Bacillus subtilis. Gene. 1986;48(2-3):301–306. doi: 10.1016/0378-1119(86)90090-9. [DOI] [PubMed] [Google Scholar]
  19. Henner D. J. Inducible expression of regulatory genes in Bacillus subtilis. Methods Enzymol. 1990;185:223–228. doi: 10.1016/0076-6879(90)85022-g. [DOI] [PubMed] [Google Scholar]
  20. Illing N., Errington J. The spoIIIA operon of Bacillus subtilis defines a new temporal class of mother-cell-specific sporulation genes under the control of the sigma E form of RNA polymerase. Mol Microbiol. 1991 Aug;5(8):1927–1940. doi: 10.1111/j.1365-2958.1991.tb00816.x. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Jaacks K. J., Healy J., Losick R., Grossman A. D. Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis. J Bacteriol. 1989 Aug;171(8):4121–4129. doi: 10.1128/jb.171.8.4121-4129.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Kudoh J., Ikeuchi T., Kurahashi K. Nucleotide sequences of the sporulation gene spo0A and its mutant genes of Bacillus subtilis. Proc Natl Acad Sci U S A. 1985 May;82(9):2665–2668. doi: 10.1073/pnas.82.9.2665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kunkel B., Kroos L., Poth H., Youngman P., Losick R. Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis. Genes Dev. 1989 Nov;3(11):1735–1744. doi: 10.1101/gad.3.11.1735. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. LaBell T. L., Trempy J. E., Haldenwang W. G. Sporulation-specific sigma factor sigma 29 of Bacillus subtilis is synthesized from a precursor protein, P31. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1784–1788. doi: 10.1073/pnas.84.7.1784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Leighton T. New types of RNA polymerase mutations causing temperature-sensitive sporulation in bacillus subtilis. J Biol Chem. 1977 Jan 10;252(1):268–272. [PubMed] [Google Scholar]
  29. Love P. E., Lyle M. J., Yasbin R. E. DNA-damage-inducible (din) loci are transcriptionally activated in competent Bacillus subtilis. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6201–6205. doi: 10.1073/pnas.82.18.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lu S., Halberg R., Kroos L. Processing of the mother-cell sigma factor, sigma K, may depend on events occurring in the forespore during Bacillus subtilis development. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9722–9726. doi: 10.1073/pnas.87.24.9722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Perego M., Cole S. P., Burbulys D., Trach K., Hoch J. A. Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J Bacteriol. 1989 Nov;171(11):6187–6196. doi: 10.1128/jb.171.11.6187-6196.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Perego M., Spiegelman G. B., Hoch J. A. Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol Microbiol. 1988 Nov;2(6):689–699. doi: 10.1111/j.1365-2958.1988.tb00079.x. [DOI] [PubMed] [Google Scholar]
  33. Popham D. L., Stragier P. Cloning, characterization, and expression of the spoVB gene of Bacillus subtilis. J Bacteriol. 1991 Dec;173(24):7942–7949. doi: 10.1128/jb.173.24.7942-7949.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rather P. N., Hay R. E., Ray G. L., Haldenwang W. G., Moran C. P., Jr Nucleotide sequences that define promoters that are used by Bacillus subtilis sigma-29 RNA polymerase. J Mol Biol. 1986 Dec 5;192(3):557–565. doi: 10.1016/0022-2836(86)90276-7. [DOI] [PubMed] [Google Scholar]
  35. Ricca E., Cutting S., Losick R. Characterization of bofA, a gene involved in intercompartmental regulation of pro-sigma K processing during sporulation in Bacillus subtilis. J Bacteriol. 1992 May;174(10):3177–3184. doi: 10.1128/jb.174.10.3177-3184.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Roels S., Driks A., Losick R. Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis. J Bacteriol. 1992 Jan;174(2):575–585. doi: 10.1128/jb.174.2.575-585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rong S., Rosenkrantz M. S., Sonenshein A. L. Transcriptional control of the Bacillus subtilis spoIID gene. J Bacteriol. 1986 Mar;165(3):771–779. doi: 10.1128/jb.165.3.771-779.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rudner D. Z., LeDeaux J. R., Ireton K., Grossman A. D. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol. 1991 Feb;173(4):1388–1398. doi: 10.1128/jb.173.4.1388-1398.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Sandman K., Losick R., Youngman P. Genetic analysis of Bacillus subtilis spo mutations generated by Tn917-mediated insertional mutagenesis. Genetics. 1987 Dec;117(4):603–617. doi: 10.1093/genetics/117.4.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Satola S., Kirchman P. A., Moran C. P., Jr Spo0A binds to a promoter used by sigma A RNA polymerase during sporulation in Bacillus subtilis. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4533–4537. doi: 10.1073/pnas.88.10.4533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schaeffer P., Millet J., Aubert J. P. Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A. 1965 Sep;54(3):704–711. doi: 10.1073/pnas.54.3.704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Stragier P., Losick R. Cascades of sigma factors revisited. Mol Microbiol. 1990 Nov;4(11):1801–1806. doi: 10.1111/j.1365-2958.1990.tb02028.x. [DOI] [PubMed] [Google Scholar]
  46. Strauch M., Webb V., Spiegelman G., Hoch J. A. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1801–1805. doi: 10.1073/pnas.87.5.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Vasantha N., Freese E. Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides. J Bacteriol. 1980 Dec;144(3):1119–1125. doi: 10.1128/jb.144.3.1119-1125.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Weinrauch Y., Penchev R., Dubnau E., Smith I., Dubnau D. A Bacillus subtilis regulatory gene product for genetic competence and sporulation resembles sensor protein members of the bacterial two-component signal-transduction systems. Genes Dev. 1990 May;4(5):860–872. doi: 10.1101/gad.4.5.860. [DOI] [PubMed] [Google Scholar]
  49. Youngman P., Perkins J. B., Losick R. A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions. Mol Gen Genet. 1984;195(3):424–433. doi: 10.1007/BF00341443. [DOI] [PubMed] [Google Scholar]
  50. Youngman P., Perkins J. B., Losick R. Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposon-borne erm gene. Plasmid. 1984 Jul;12(1):1–9. doi: 10.1016/0147-619x(84)90061-1. [DOI] [PubMed] [Google Scholar]
  51. Zheng L. B., Losick R. Cascade regulation of spore coat gene expression in Bacillus subtilis. J Mol Biol. 1990 Apr 20;212(4):645–660. doi: 10.1016/0022-2836(90)90227-d. [DOI] [PubMed] [Google Scholar]

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

RESOURCES