Abstract
A hallmark of sporulation of Bacillus subtilis is the formation of two distinct cells by an asymmetric division. The development programs in these two cells involve the compartmentalized activities of sigma E in the larger mother cell and of sigma F in the smaller prespore. Activation of sigma E requires expression of the sigma F-directed gene spoIIR. By immunofluorescence microscopy of a strain containing a spoIIR-lacZ fusion, we have shown that spoIIR is transcribed exclusively in the prespore. By placing spoIIR under the control of PspoIIE, it was possible to express spoIIR before the spore septum was formed. Strains containing the PspoIIE-spoIIR construct activated sigma E only in the mother cell in organisms that underwent the asymmetric sporulation division. Thus, compartmentalization of sigma E activity did not require the compartmentalization of spoIIR expression. Nor did the compartmentalization of sigma E require SpoIIAA, SpoIIAB, sigma F, or sigma F-dependent transcription, all of which are required for prespore-specific gene expression. It is inferred that although sigma F and sigma E direct compartmentalized gene expression, neither of these sigma factors, nor the genes under their control, directs the process of compartmentalization.
Full Text
The Full Text of this article is available as a PDF (416.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Beall B., Lutkenhaus J. FtsZ in Bacillus subtilis is required for vegetative septation and for asymmetric septation during sporulation. Genes Dev. 1991 Mar;5(3):447–455. doi: 10.1101/gad.5.3.447. [DOI] [PubMed] [Google Scholar]
- 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]
- Diederich B., Tatti K. M., Jones C. H., Beall B., Moran C. P., Jr Genetic suppression analysis of sigma E interaction with three promoters in sporulating Bacillus subtilis. Gene. 1992 Nov 2;121(1):63–69. doi: 10.1016/0378-1119(92)90162-i. [DOI] [PubMed] [Google Scholar]
- 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]
- Ferrari E., Henner D. J., Perego M., Hoch J. A. Transcription of Bacillus subtilis subtilisin and expression of subtilisin in sporulation mutants. J Bacteriol. 1988 Jan;170(1):289–295. doi: 10.1128/jb.170.1.289-295.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Haldenwang W. G. The sigma factors of Bacillus subtilis. Microbiol Rev. 1995 Mar;59(1):1–30. doi: 10.1128/mr.59.1.1-30.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harry E. J., Pogliano K., Losick R. Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis. J Bacteriol. 1995 Jun;177(12):3386–3393. doi: 10.1128/jb.177.12.3386-3393.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins M. L., Piggot P. J. Septal membrane fusion--a pivotal event in bacterial spore formation? Mol Microbiol. 1992 Sep;6(18):2565–2571. doi: 10.1111/j.1365-2958.1992.tb01433.x. [DOI] [PubMed] [Google Scholar]
- Hofmeister A. E., Londoño-Vallejo A., Harry E., Stragier P., Losick R. Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. subtilis. Cell. 1995 Oct 20;83(2):219–226. doi: 10.1016/0092-8674(95)90163-9. [DOI] [PubMed] [Google Scholar]
- Illing N., Errington J. Genetic regulation of morphogenesis in Bacillus subtilis: roles of sigma E and sigma F in prespore engulfment. J Bacteriol. 1991 May;173(10):3159–3169. doi: 10.1128/jb.173.10.3159-3169.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Jonas R. M., Peters H. K., 3rd, Haldenwang W. G. Phenotypes of Bacillus subtilis mutants altered in the precursor-specific region of sigma E. J Bacteriol. 1990 Aug;172(8):4178–4186. doi: 10.1128/jb.172.8.4178-4186.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jonas R. M., Weaver E. A., Kenney T. J., Moran C. P., Jr, Haldenwang W. G. The Bacillus subtilis spoIIG operon encodes both sigma E and a gene necessary for sigma E activation. J Bacteriol. 1988 Feb;170(2):507–511. doi: 10.1128/jb.170.2.507-511.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karow M. L., Glaser P., Piggot P. J. Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2012–2016. doi: 10.1073/pnas.92.6.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karow M. L., Piggot P. J. Construction of gusA transcriptional fusion vectors for Bacillus subtilis and their utilization for studies of spore formation. Gene. 1995 Sep 22;163(1):69–74. doi: 10.1016/0378-1119(95)00402-r. [DOI] [PubMed] [Google Scholar]
- Levin P. A., Losick R. Characterization of a cell division gene from Bacillus subtilis that is required for vegetative and sporulation septum formation. J Bacteriol. 1994 Mar;176(5):1451–1459. doi: 10.1128/jb.176.5.1451-1459.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis P. J., Partridge S. R., Errington J. Sigma factors, asymmetry, and the determination of cell fate in Bacillus subtilis. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3849–3853. doi: 10.1073/pnas.91.9.3849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Londoño-Vallejo J. A., Stragier P. Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis. Genes Dev. 1995 Feb 15;9(4):503–508. doi: 10.1101/gad.9.4.503. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Masuda E. S., Anaguchi H., Sato T., Takeuchi M., Kobayashi Y. Nucleotide sequence of the sporulation gene spoIIGA from Bacillus subtilis. Nucleic Acids Res. 1990 Feb 11;18(3):657–657. doi: 10.1093/nar/18.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mueller J. P., Bukusoglu G., Sonenshein A. L. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol. 1992 Jul;174(13):4361–4373. doi: 10.1128/jb.174.13.4361-4373.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Santana M., Ionescu M. S., Vertes A., Longin R., Kunst F., Danchin A., Glaser P. Bacillus subtilis F0F1 ATPase: DNA sequence of the atp operon and characterization of atp mutants. J Bacteriol. 1994 Nov;176(22):6802–6811. doi: 10.1128/jb.176.22.6802-6811.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Setlow B., Magill N., Febbroriello P., Nakhimovsky L., Koppel D. E., Setlow P. Condensation of the forespore nucleoid early in sporulation of Bacillus species. J Bacteriol. 1991 Oct;173(19):6270–6278. doi: 10.1128/jb.173.19.6270-6278.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- York K., Kenney T. J., Satola S., Moran C. P., Jr, Poth H., Youngman P. Spo0A controls the sigma A-dependent activation of Bacillus subtilis sporulation-specific transcription unit spoIIE. J Bacteriol. 1992 Apr;174(8):2648–2658. doi: 10.1128/jb.174.8.2648-2658.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]