The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence (original) (raw)
Abstract
Spore formation in Bacillus subtilis is a dramatic response to environmental signals that is controlled in part by a two-component regulatory system composed of a histidine protein kinase (SpoIIJ) and a transcriptional regulator (Spo0A). The spo0K locus plays an important but undefined role in the initiation of sporulation and in the development of genetic competence. spoIIJ spo0K double mutants had a more severe defect in sporulation than either single mutant. Overproduction of the spoIIJ gene product resulted in the suppression of the sporulation defect, but not the competence defect, caused by mutations in the spo0K locus. On the basis of the phenotype of the spoIIJ spo0K double mutant and the effect of overproduction of the spoIIJ gene product, a transposon insertion in the spo0K locus was isolated. The spo0K locus was cloned and sequenced. spo0K proved to be an operon of five genes that is homologous to the oligopeptide permease (opp) operon of Salmonella typhimurium and related to a large family of membrane transport systems. The requirement for the transport system encoded by spo0K in the development of competence was somewhat different than its requirement in the system encoded by spo0K in the development of competence was somewhat different than its requirement in the initiation of sporulation. Disruption of the last open reading frame in the spo0K operon caused a defect in competence but had little or no effect on sporulation. We hypothesize that the transport system encoded by spo0K may have a role in sensing extracellular peptide factors that we have shown are required for efficient sporulation and perhaps in sensing similar factors that may be necessary for genetic competence.
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akrigg A., Ayad S. R., Barker G. R. The nature of a competence-inducing factor in Bacillus subtilis. Biochem Biophys Res Commun. 1967 Sep 27;28(6):1062–1067. doi: 10.1016/0006-291x(67)90090-3. [DOI] [PubMed] [Google Scholar]
- Akrigg A., Ayad S. R. Studies on the competence-inducing factor of Bacillus subtilis. Biochem J. 1970 Apr;117(2):397–403. doi: 10.1042/bj1170397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Alloing G., Trombe M. C., Claverys J. P. The ami locus of the gram-positive bacterium Streptococcus pneumoniae is similar to binding protein-dependent transport operons of gram-negative bacteria. Mol Microbiol. 1990 Apr;4(4):633–644. doi: 10.1111/j.1365-2958.1990.tb00632.x. [DOI] [PubMed] [Google Scholar]
- Ames G. F. Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem. 1986;55:397–425. doi: 10.1146/annurev.bi.55.070186.002145. [DOI] [PubMed] [Google Scholar]
- 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]
- Blight M. A., Holland I. B. Structure and function of haemolysin B,P-glycoprotein and other members of a novel family of membrane translocators. Mol Microbiol. 1990 Jun;4(6):873–880. doi: 10.1111/j.1365-2958.1990.tb00660.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Coote J. G. Sporulation in Bacillus subtilis. Characterization of oligosporogenous mutants and comparison of their phenotypes with those of asporogenous mutants. J Gen Microbiol. 1972 Jun;71(1):1–15. doi: 10.1099/00221287-71-1-1. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Gilson E., Alloing G., Schmidt T., Claverys J. P., Dudler R., Hofnung M. Evidence for high affinity binding-protein dependent transport systems in gram-positive bacteria and in Mycoplasma. EMBO J. 1988 Dec 1;7(12):3971–3974. doi: 10.1002/j.1460-2075.1988.tb03284.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodell E. W., Higgins C. F. Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. J Bacteriol. 1987 Aug;169(8):3861–3865. doi: 10.1128/jb.169.8.3861-3865.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grossman A. D., Losick R. Extracellular control of spore formation in Bacillus subtilis. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4369–4373. doi: 10.1073/pnas.85.12.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Higgins C. F., Hiles I. D., Salmond G. P., Gill D. R., Downie J. A., Evans I. J., Holland I. B., Gray L., Buckel S. D., Bell A. W. A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature. 1986 Oct 2;323(6087):448–450. doi: 10.1038/323448a0. [DOI] [PubMed] [Google Scholar]
- Hiles I. D., Gallagher M. P., Jamieson D. J., Higgins C. F. Molecular characterization of the oligopeptide permease of Salmonella typhimurium. J Mol Biol. 1987 May 5;195(1):125–142. doi: 10.1016/0022-2836(87)90332-9. [DOI] [PubMed] [Google Scholar]
- Hoch J. A., Trach K., Kawamura F., Saito H. Identification of the transcriptional suppressor sof-1 as an alteration in the spo0A protein. J Bacteriol. 1985 Feb;161(2):552–555. doi: 10.1128/jb.161.2.552-555.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyde S. C., Emsley P., Hartshorn M. J., Mimmack M. M., Gileadi U., Pearce S. R., Gallagher M. P., Gill D. R., Hubbard R. E., Higgins C. F. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature. 1990 Jul 26;346(6282):362–365. doi: 10.1038/346362a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Joenje H., Gruber M., Venema G. Stimulation of the development of competence by culture fluids in Bacillus subtilis transformation. Biochim Biophys Acta. 1972 Mar 14;262(2):189–199. doi: 10.1016/0005-2787(72)90232-8. [DOI] [PubMed] [Google Scholar]
- Kim S. K., Kaiser D. C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell. 1990 Apr 6;61(1):19–26. doi: 10.1016/0092-8674(90)90211-v. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- McGrath J. P., Varshavsky A. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature. 1989 Aug 3;340(6232):400–404. doi: 10.1038/340400a0. [DOI] [PubMed] [Google Scholar]
- Mimmack M. L., Gallagher M. P., Pearce S. R., Hyde S. C., Booth I. R., Higgins C. F. Energy coupling to periplasmic binding protein-dependent transport systems: stoichiometry of ATP hydrolysis during transport in vivo. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8257–8261. doi: 10.1073/pnas.86.21.8257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morrison D. A., Baker M. F. Competence for genetic transformation in pneumococcus depends on synthesis of a small set of proteins. Nature. 1979 Nov 8;282(5735):215–217. doi: 10.1038/282215a0. [DOI] [PubMed] [Google Scholar]
- Msadek T., Kunst F., Henner D., Klier A., Rapoport G., Dedonder R. Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol. 1990 Feb;172(2):824–834. doi: 10.1128/jb.172.2.824-834.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nixon B. T., Ronson C. W., Ausubel F. M. Two-component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7850–7854. doi: 10.1073/pnas.83.20.7850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Perego M., Hoch J. A. Sequence analysis and regulation of the hpr locus, a regulatory gene for protease production and sporulation in Bacillus subtilis. J Bacteriol. 1988 Jun;170(6):2560–2567. doi: 10.1128/jb.170.6.2560-2567.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Rao N. N., Torriani A. Molecular aspects of phosphate transport in Escherichia coli. Mol Microbiol. 1990 Jul;4(7):1083–1090. doi: 10.1111/j.1365-2958.1990.tb00682.x. [DOI] [PubMed] [Google Scholar]
- Roggiani M., Hahn J., Dubnau D. Suppression of early competence mutations in Bacillus subtilis by mec mutations. J Bacteriol. 1990 Jul;172(7):4056–4063. doi: 10.1128/jb.172.7.4056-4063.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sadaie Y., Kada T. Formation of competent Bacillus subtilis cells. J Bacteriol. 1983 Feb;153(2):813–821. doi: 10.1128/jb.153.2.813-821.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Shoji K., Hiratsuka S., Kawamura F., Kobayashi Y. New suppressor mutation sur0B of spo0B and spo0F mutations in Bacillus subtilis. J Gen Microbiol. 1988 Dec;134(12):3249–3257. doi: 10.1099/00221287-134-12-3249. [DOI] [PubMed] [Google Scholar]
- Spiegelman G., Van Hoy B., Perego M., Day J., Trach K., Hoch J. A. Structural alterations in the Bacillus subtilis Spo0A regulatory protein which suppress mutations at several spo0 loci. J Bacteriol. 1990 Sep;172(9):5011–5019. doi: 10.1128/jb.172.9.5011-5019.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- TOMASZ A., HOTCHKISS R. D. REGULATION OF THE TRANSFORMABILITY OF PHEUMOCOCCAL CULTURES BY MACROMOLECULAR CELL PRODUCTS. Proc Natl Acad Sci U S A. 1964 Mar;51:480–487. doi: 10.1073/pnas.51.3.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Vasantha N., Freese E. The role of manganese in growth and sporulation of Bacillus subtilis. J Gen Microbiol. 1979 Jun;112(2):329–336. doi: 10.1099/00221287-112-2-329. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]