• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Jan 1995; 177(1): 166–175.
PMCID: PMC176569

Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis.

Abstract

Phosphorylation of the transcription factor encoded by spo0A is required for the initiation of sporulation in Bacillus subtilis. Production and accumulation of Spo0A-P is controlled by histidine protein kinases and the spo0 gene products. To identify additional genes that might be involved in the initiation of sporulation and production of Spo0A-P, we isolated genes which when present on a multicopy plasmid could suppress the sporulation defect of a spo0K mutant. kinC was one gene isolated in this way. A multicopy plasmid containing kinC completely or partially suppressed the sporulation defect caused by mutations in spo0K, kinA, spo0F, and spo0B, indicating that at least when overexpressed, KinC is capable of stimulating phosphorylation of Spo0A independently of the normal phosphorylation pathway. The predicted product of kinC is 428 amino acids long and is most similar to KinA and KinB, the histidine protein kinases involved in the initiation of sporulation. In otherwise wild-type strains, kinC null mutations caused little or no defect in sporulation under the conditions tested. However, in the absence of a functional phosphorelay (spo0F or spo0B), KinC appears to be the kinase responsible for phosphorylation of the sof-1 and rvtA11 forms of Spo0A.

Full Text

The Full Text of this article is available as a PDF (366K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Albright LM, Huala E, Ausubel FM. Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu Rev Genet. 1989;23:311–336. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Baldus JM, Green BD, Youngman P, Moran CP., Jr Phosphorylation of Bacillus subtilis transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes. J Bacteriol. 1994 Jan;176(2):296–306. [PMC free article] [PubMed]
  • Benson AK, Haldenwang WG. Regulation of sigma B levels and activity in Bacillus subtilis. J Bacteriol. 1993 Apr;175(8):2347–2356. [PMC free article] [PubMed]
  • Bird TH, Grimsley JK, Hoch JA, Spiegelman GB. Phosphorylation of Spo0A activates its stimulation of in vitro transcription from the Bacillus subtilis spoIIG operon. Mol Microbiol. 1993 Aug;9(4):741–749. [PubMed]
  • Boylan SA, Chun KT, Edson BA, Price CW. Early-blocked sporulation mutations alter expression of enzymes under carbon control in Bacillus subtilis. Mol Gen Genet. 1988 May;212(2):271–280. [PubMed]
  • Burbulys D, Trach KA, Hoch JA. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell. 1991 Feb 8;64(3):545–552. [PubMed]
  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. [PubMed]
  • Chung JD, Stephanopoulos G, Ireton K, Grossman AD. Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation. J Bacteriol. 1994 Apr;176(7):1977–1984. [PMC free article] [PubMed]
  • Dedonder RA, Lepesant JA, Lepesant-Kejzlarová J, Billault A, Steinmetz M, Kunst F. Construction of a kit of reference strains for rapid genetic mapping in Bacillus subtilis 168. Appl Environ Microbiol. 1977 Apr;33(4):989–993. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Ferrari FA, Nguyen A, Lang D, Hoch JA. Construction and properties of an integrable plasmid for Bacillus subtilis. J Bacteriol. 1983 Jun;154(3):1513–1515. [PMC free article] [PubMed]
  • Grossman AD, Lewis T, Levin N, DeVivo R. Suppressors of a spo0A missense mutation and their effects on sporulation in Bacillus subtilis. Biochimie. 1992 Jul-Aug;74(7-8):679–688. [PubMed]
  • Gryczan T, Contente S, Dubnau D. Molecular cloning of heterologous chromosomal DNA by recombination between a plasmid vector and a homologous resident plasmid in Bacillus subtilis. Mol Gen Genet. 1980 Feb;177(3):459–467. [PubMed]
  • Haima P, Bron S, Venema G. The effect of restriction on shotgun cloning and plasmid stability in Bacillus subtilis Marburg. Mol Gen Genet. 1987 Sep;209(2):335–342. [PubMed]
  • Henner DJ. Inducible expression of regulatory genes in Bacillus subtilis. Methods Enzymol. 1990;185:223–228. [PubMed]
  • Hoch JA. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu Rev Microbiol. 1993;47:441–465. [PubMed]
  • Hoch JA, 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. [PMC free article] [PubMed]
  • Ireton K, Grossman AD. Coupling between gene expression and DNA synthesis early during development in Bacillus subtilis. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8808–8812. [PMC free article] [PubMed]
  • Ireton K, Grossman AD. Interactions among mutations that cause altered timing of gene expression during sporulation in Bacillus subtilis. J Bacteriol. 1992 May;174(10):3185–3195. [PMC free article] [PubMed]
  • Ireton K, Grossman AD. A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis. EMBO J. 1994 Apr 1;13(7):1566–1573. [PMC free article] [PubMed]
  • Ireton K, Gunther NW, 4th, Grossman AD. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol. 1994 Sep;176(17):5320–5329. [PMC free article] [PubMed]
  • Ireton K, Rudner DZ, Siranosian KJ, Grossman AD. Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev. 1993 Feb;7(2):283–294. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Jaacks KJ, Healy J, Losick R, Grossman AD. Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis. J Bacteriol. 1989 Aug;171(8):4121–4129. [PMC free article] [PubMed]
  • Kawamura F, Saito H. Isolation and mapping of a new suppressor mutation of an early sporulation gene spoOF mutation in Bacillus subtilis. Mol Gen Genet. 1983;192(3):330–334. [PubMed]
  • Kenney TJ, Moran CP., Jr Organization and regulation of an operon that encodes a sporulation-essential sigma factor in Bacillus subtilis. J Bacteriol. 1987 Jul;169(7):3329–3339. [PMC free article] [PubMed]
  • Kobayashi K, Shoji K, Shimizu T, Nakano K, Sato T, Kobayashi Y. Analysis of a suppressor mutation ssb (kinC) of sur0B20 (spo0A) mutation in Bacillus subtilis reveals that kinC encodes a histidine protein kinase. J Bacteriol. 1995 Jan;177(1):176–182. [PMC free article] [PubMed]
  • 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]
  • Magnuson R, Solomon J, Grossman AD. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell. 1994 Apr 22;77(2):207–216. [PubMed]
  • Ohlsen KL, Grimsley JK, Hoch JA. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1756–1760. [PMC free article] [PubMed]
  • Ota IM, Varshavsky A. A yeast protein similar to bacterial two-component regulators. Science. 1993 Oct 22;262(5133):566–569. [PubMed]
  • Parkinson JS, Kofoid EC. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. [PubMed]
  • Perego M, Cole SP, Burbulys D, Trach K, Hoch JA. 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. [PMC free article] [PubMed]
  • Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol. 1991 Jan;5(1):173–185. [PubMed]
  • Perego M, Hoch JA. Isolation and sequence of the spo0E gene: its role in initiation of sporulation in Bacillus subtilis. Mol Microbiol. 1987 Jul;1(1):125–132. [PubMed]
  • Perego M, Hoch JA. Negative regulation of Bacillus subtilis sporulation by the spo0E gene product. J Bacteriol. 1991 Apr;173(8):2514–2520. [PMC free article] [PubMed]
  • Perego M, Spiegelman GB, Hoch JA. 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. [PubMed]
  • Piggot PJ, Coote JG. Genetic aspects of bacterial endospore formation. Bacteriol Rev. 1976 Dec;40(4):908–962. [PMC free article] [PubMed]
  • Robertson JB, Gocht M, Marahiel MA, Zuber P. AbrB, a regulator of gene expression in Bacillus, interacts with the transcription initiation regions of a sporulation gene and an antibiotic biosynthesis gene. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8457–8461. [PMC free article] [PubMed]
  • Rudner DZ, LeDeaux JR, Ireton K, Grossman AD. 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. [PMC free article] [PubMed]
  • Sadaie Y, Kada T. Formation of competent Bacillus subtilis cells. J Bacteriol. 1983 Feb;153(2):813–821. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Satola S, Kirchman PA, Moran CP., 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. [PMC free article] [PubMed]
  • Satola SW, Baldus JM, Moran CP., Jr Binding of Spo0A stimulates spoIIG promoter activity in Bacillus subtilis. J Bacteriol. 1992 Mar;174(5):1448–1453. [PMC free article] [PubMed]
  • Schaeffer P, Millet J, Aubert JP. Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A. 1965 Sep;54(3):704–711. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Spiegelman G, Van Hoy B, Perego M, Day J, Trach K, Hoch JA. Structural alterations in the Bacillus subtilis Spo0A regulatory protein which suppress mutations at several spo0 loci. J Bacteriol. 1990 Sep;172(9):5011–5019. [PMC free article] [PubMed]
  • Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1072–1078. [PMC free article] [PubMed]
  • Strauch MA, Spiegelman GB, Perego M, Johnson WC, Burbulys D, Hoch JA. The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. EMBO J. 1989 May;8(5):1615–1621. [PMC free article] [PubMed]
  • Strauch M, Webb V, Spiegelman G, Hoch JA. 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. [PMC free article] [PubMed]
  • Trach K, Burbulys D, Strauch M, Wu JJ, Dhillon N, Jonas R, Hanstein C, Kallio P, Perego M, Bird T, et al. Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. Res Microbiol. 1991 Sep-Oct;142(7-8):815–823. [PubMed]
  • Trach KA, Hoch JA. Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway. Mol Microbiol. 1993 Apr;8(1):69–79. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Wu JJ, Howard MG, Piggot PJ. Regulation of transcription of the Bacillus subtilis spoIIA locus. J Bacteriol. 1989 Feb;171(2):692–698. [PMC free article] [PubMed]
  • Yansura DG, Henner DJ. 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. [PMC free article] [PubMed]
  • York K, Kenney TJ, Satola S, Moran CP, 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. [PMC free article] [PubMed]
  • Zuber P, Losick R. Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis. J Bacteriol. 1987 May;169(5):2223–2230. [PMC free article] [PubMed]

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

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...