Home LiteratureArticle Details
PMID: 10348850 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Role of SpoVG in asymmetric septation in Bacillus subtilis.

Journal of bacteriology ·Vol. 181 ·No. 11 ·1999-06-00 ·Pages 3392-401

Matsuno K, Sonenshein AL

Abstract

Deletion of the citC gene, coding for isocitrate dehydrogenase, arrests sporulation of Bacillus subtilis at stage I after bipolar localization of the cell division protein FtsZ but before formation of the asymmetric septum. A spontaneous extragenic suppressor mutation that overcame the stage I block was found to map within the spoVG gene. The suppressing mutation and other spoVG loss-of-function mutations enabled citC mutant cells to form asymmetric septa and to activate the forespore-specific sigma factor sigmaF. However, little induction of mother cell-specific, sigmaE-dependent sporulation genes was observed in a citC spoVG double mutant, indicating that there is an additional defect(s) in compartmentalized gene expression in the citC mutant. These other defects could be partially overcome by reducing the synthesis of citrate, by buffering the medium, or by adding excess MnCl2. Overexpression of the spoVG gene in wild-type cells significantly delayed sigmaF activation. Increased expression and stability of SpoVG in citC mutant cells may contribute to the citC mutant phenotype. Inactivation of the spoVG gene caused a population of otherwise wild-type cells to produce a small number of minicells during growth and caused sporulating cells to complete asymmetric septation more rapidly than normal. Unlike the case for inactivation of the cell division inhibitor gene minD, many of these minicells contained DNA and appeared only when the primary sporulation signal transduction pathway, the Spo0A phosphorelay, was active. These results suggest that SpoVG interferes with or is a negative regulator of the pathway leading to asymmetric septation.

MeSH Terms
Bacillus subtilis/enzymology,genetics,physiology,ultrastructure Bacterial Proteins/genetics,physiology Cell Division Cell Wall/metabolism,ultrastructure Citric Acid Cycle/genetics Cloning, Molecular DNA Mutational Analysis Gene Deletion Gene Expression/genetics Genes, Recessive/genetics Genes, Reporter/genetics Isocitrate Dehydrogenase/genetics,metabolism Microscopy, Electron Sigma Factor/physiology Spores, Bacterial/physiology Suppression, Genetic/genetics Transcription Factors
Chemicals
Bacterial Proteins Sigma Factor SpoVG protein, Bacillus subtilis Transcription Factors spoIIR protein, Bacillus subtilis spore-specific proteins, Bacillus Isocitrate Dehydrogenase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Matsuno K
Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, Massachusetts 02111, USA.
Sonenshein A L
References (68)
68 references, click to expand
  1. Transcriptional regulation of a Bacillus subtilis dipeptide transport operon.
    Mol Microbiol. 1991 Aug;5(8):1915-25 PMID: 1766371
  2. Analysis of sporulation mutants. II. Mutants blocked in the citric acid cycle.
    J Bacteriol. 1968 Apr;95(4):1431-8 PMID: 4967197
  3. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance.
    Biochem J. 1969 Jun;113(1):29-37 PMID: 4185146
  4. An improved and rapid procedure for isolating RNA-free Escherichia coli plasmid DNA.
    Genet Anal Tech Appl. 1991 May;8(3):107-10 PMID: 1712213
  5. Condensation of the forespore nucleoid early in sporulation of Bacillus species.
    J Bacteriol. 1991 Oct;173(19):6270-8 PMID: 1917859
  6. 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):1237-56 PMID: 1942049
  7. FtsZ ring structure associated with division in Escherichia coli.
    Nature. 1991 Nov 14;354(6349):161-4 PMID: 1944597
  8. Citric acid cycle: gene-enzyme relationships in Bacillus subtilis.
    J Bacteriol. 1970 Nov;104(2):826-33 PMID: 4992371
  9. 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):209-21 PMID: 4994568
  10. Sporulation of tricarboxylic acid cycle mutants of Bacillus subtilis.
    J Bacteriol. 1972 Feb;109(2):886-94 PMID: 4110146
  11. Developmental block in citric acid cycle mutants of Bacillus subtilis.
    J Bacteriol. 1973 Dec;116(3):1466-8 PMID: 4201776
  12. Genetic aspects of bacterial endospore formation.
    Bacteriol Rev. 1976 Dec;40(4):908-62 PMID: 12736
  13. Cloned Bacillus subtilis DNA containing a gene that is activated early during sporulation.
    Cell. 1977 Aug;11(4):751-61 PMID: 408013
  14. Mapping a cloned gene under sporulation control by inserttion of a drug resistance marker into the Bacillus subtilis chromosome.
    J Bacteriol. 1980 Apr;142(1):90-8 PMID: 6768719
  15. Developmentally regulated transcription in a cloned segment of the Bacillus subtilis chromosome.
    J Bacteriol. 1981 Aug;147(2):432-42 PMID: 6790515
  16. Identification of a new developmental locus in Bacillus subtilis by construction of a deletion mutation in a cloned gene under sporulation control.
    J Bacteriol. 1981 Oct;148(1):341-51 PMID: 6793556
  17. Deletion analysis of a complex promoter for a developmentally regulated gene from Bacillus subtilis.
    J Mol Biol. 1983 Aug 5;168(2):351-65 PMID: 6411929
  18. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  19. Transcriptional control of the Bacillus subtilis spoIID gene.
    J Bacteriol. 1986 Mar;165(3):771-9 PMID: 2419309
  20. Effects of plasmid propagation of a sporulation promoter on promoter utilization and sporulation in Bacillus subtilis.
    J Bacteriol. 1987 Feb;169(2):461-9 PMID: 3027029
  21. The effect of restriction on shotgun cloning and plasmid stability in Bacillus subtilis Marburg.
    Mol Gen Genet. 1987 Sep;209(2):335-42 PMID: 2823077
  22. Genetic analysis of Bacillus subtilis spo mutations generated by Tn917-mediated insertional mutagenesis.
    Genetics. 1987 Dec;117(4):603-17 PMID: 2828153
  23. Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli.
    J Bacteriol. 1988 May;170(5):2106-12 PMID: 2834323
  24. 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):4361-73 PMID: 1378051
  25. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein.
    Nature. 1992 Sep 17;359(6392):251-4 PMID: 1528267
  26. The essential bacterial cell-division protein FtsZ is a GTPase.
    Nature. 1992 Sep 17;359(6392):254-6 PMID: 1528268
  27. Identification of Bacillus subtilis genes for septum placement and shape determination.
    J Bacteriol. 1992 Nov;174(21):6717-28 PMID: 1400224
  28. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants.
    J Bacteriol. 1992 Nov;174(21):6729-42 PMID: 1400225
  29. Sporulation gene spoIIB from Bacillus subtilis.
    J Bacteriol. 1993 Jan;175(2):528-40 PMID: 8419299
  30. Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor.
    Genes Dev. 1993 Feb;7(2):283-94 PMID: 8436298
  31. The minCD locus of Bacillus subtilis lacks the minE determinant that provides topological specificity to cell division.
    Mol Microbiol. 1993 Feb;7(4):601-10 PMID: 8459776
  32. Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon.
    J Bacteriol. 1993 Aug;175(15):4605-14 PMID: 8335620
  33. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase.
    Cell. 1993 Aug 27;74(4):735-42 PMID: 8358793
  34. Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis.
    J Bacteriol. 1995 Jan;177(1):166-75 PMID: 8002614
  35. Identification and characterization of the Bacillus subtilis spoIIP locus.
    J Bacteriol. 1995 Feb;177(3):716-22 PMID: 7836306
  36. Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis.
    Genes Dev. 1995 Feb 15;9(4):503-8 PMID: 7883171
  37. 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):2012-6 PMID: 7892217
  38. Krebs cycle function is required for activation of the Spo0A transcription factor in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2845-9 PMID: 7708735
  39. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis.
    Genes Dev. 1995 Jun 1;9(11):1316-26 PMID: 7797072
  40. Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. subtilis.
    Cell. 1995 Oct 20;83(2):219-26 PMID: 7585939
  41. Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division.
    Science. 1995 Oct 27;270(5236):641-4 PMID: 7570023
  42. Systematic sequencing of the 180 kilobase region of the Bacillus subtilis chromosome containing the replication origin.
    DNA Res. 1994;1(1):1-14 PMID: 7584024
  43. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis.
    Genes Dev. 1996 Feb 15;10(4):478-88 PMID: 8600030
  44. Characterization of the major citrate synthase of Bacillus subtilis.
    J Bacteriol. 1996 Jun;178(12):3658-60 PMID: 8655569
  45. Plasmids for ectopic integration in Bacillus subtilis.
    Gene. 1996 Nov 21;180(1-2):57-61 PMID: 8973347
  46. Molecular genetics of sporulation in Bacillus subtilis.
    Annu Rev Genet. 1996;30:297-41 PMID: 8982457
  47. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli.
    Cell. 1997 Jan 24;88(2):175-85 PMID: 9008158
  48. SpoIIQ, a forespore-expressed gene required for engulfment in Bacillus subtilis.
    Mol Microbiol. 1997 Apr;24(1):29-39 PMID: 9140963
  49. Deletion of the Bacillus subtilis isocitrate dehydrogenase gene causes a block at stage I of sporulation.
    J Bacteriol. 1997 Aug;179(15):4725-32 PMID: 9244258
  50. An lrp-like gene of Bacillus subtilis involved in branched-chain amino acid transport.
    J Bacteriol. 1997 Sep;179(17):5448-57 PMID: 9287000
  51. A null mutation in the Bacillus subtilis aconitase gene causes a block in Spo0A-phosphate-dependent gene expression.
    J Bacteriol. 1997 Dec;179(23):7351-9 PMID: 9393699
  52. The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli.
    Cell. 1997 Nov 28;91(5):685-94 PMID: 9393861
  53. Effect of minCD on FtsZ ring position and polar septation in Bacillus subtilis.
    J Bacteriol. 1998 Nov;180(22):6048-51 PMID: 9811667
  54. Metabolic imbalance and sporulation in an isocitrate dehydrogenase mutant of Bacillus subtilis.
    J Bacteriol. 1999 Jun;181(11):3382-91 PMID: 10348849
  55. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis.
    Cell. 1994 Apr 22;77(2):195-205 PMID: 8168129
  56. 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):461-73 PMID: 3135411
  57. High efficiency transformation of E. coli by high voltage electroporation.
    Nucleic Acids Res. 1988 Jul 11;16(13):6127-45 PMID: 3041370
  58. 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):689-99 PMID: 3145384
  59. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli.
    Cell. 1989 Feb 24;56(4):641-9 PMID: 2645057
  60. A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis.
    J Bacteriol. 1990 Feb;172(2):835-44 PMID: 2105305
  61. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  62. 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):9722-6 PMID: 2124700
  63. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay.
    Cell. 1991 Feb 8;64(3):545-52 PMID: 1846779
  64. FtsZ in Bacillus subtilis is required for vegetative septation and for asymmetric septation during sporulation.
    Genes Dev. 1991 Mar;5(3):447-55 PMID: 1848202
  65. Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-sigma K processing in Bacillus subtilis.
    Genes Dev. 1991 Mar;5(3):456-66 PMID: 1900494
  66. Effect of promoter mutations and upstream deletions on the expression of genes coding for small, acid-soluble spore proteins of Bacillus subtilis.
    J Bacteriol. 1991 Mar;173(6):2011-6 PMID: 1900507
  67. 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):2977-84 PMID: 1902213
  68. The role of sigma F in prespore-specific transcription in Bacillus subtilis.
    Mol Microbiol. 1991 Mar;5(3):757-67 PMID: 1904527
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-06-00
Pages
3392-401
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC93805
Subset
IM
Grants
NIGMS NIH HHS · R01 GM042219 · United States
NIGMS NIH HHS · GM42219 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]