Home LiteratureArticle Details
PMID: 7708735 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Krebs cycle function is required for activation of the Spo0A transcription factor in Bacillus subtilis.

Ireton K, Jin S, Grossman AD, Sonenshein AL

Abstract

Expression of genes early during sporulation in Bacillus subtilis requires the activity of the transcription factor encoded by spo0A. The active, phosphorylated form of Spo0A is produced through the action of a multicomponent pathway, the phosphorelay. A mutant defective in the first three enzymes of the Krebs citric acid cycle was unable to express early sporulation genes, apparently because of a failure to activate the phosphorelay. Cells that produce an altered Spo0A protein that can be phosphorylated by an alternative pathway were not dependent on Krebs cycle function for early sporulation gene expression. These findings suggest that Krebs cycle enzymes transmit a signal to activate the phosphorelay and that B. subtilis monitors its metabolic potential before committing itself to spore formation.

Related Genes
MeSH Terms
Bacillus subtilis/growth & development,physiology Bacterial Proteins/biosynthesis Citric Acid Cycle Gene Deletion Gene Expression Genotype Glucose/metabolism Kinetics Mutagenesis, Insertional Phosphorylation Promoter Regions, Genetic Spores, Bacterial/physiology Transcription Factors/biosynthesis
Chemicals
Bacterial Proteins Spo0A protein, Bacillus subtilis Transcription Factors Glucose
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ireton K
Department of Biology, Massachusetts Institute of Technology, Cambridge 02139, USA.
Jin S
Grossman A D
Sonenshein A L
References (59)
59 references, click to expand
  1. Transcription of the Bacillus subtilis spoIIA locus.
    Gene. 1991 May 15;101(1):113-6 PMID: 1905664
  2. Transcriptional regulation of a Bacillus subtilis dipeptide transport operon.
    Mol Microbiol. 1991 Aug;5(8):1915-25 PMID: 1766371
  3. Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay.
    Res Microbiol. 1991 Sep-Oct;142(7-8):815-23 PMID: 1664534
  4. Binding of Spo0A stimulates spoIIG promoter activity in Bacillus subtilis.
    J Bacteriol. 1992 Mar;174(5):1448-53 PMID: 1537790
  5. Catabolic repression of bacterial sporulation.
    Proc Natl Acad Sci U S A. 1965 Sep;54(3):704-11 PMID: 4956288
  6. Analysis of sporulation mutants. II. Mutants blocked in the citric acid cycle.
    J Bacteriol. 1968 Apr;95(4):1431-8 PMID: 4967197
  7. Sporulation of Bacillus subtilis in continuous culture.
    J Bacteriol. 1970 Sep;103(3):529-35 PMID: 4990846
  8. Sporulation of tricarboxylic acid cycle mutants of Bacillus subtilis.
    J Bacteriol. 1972 Feb;109(2):886-94 PMID: 4110146
  9. Induction of sporulation in developmental mutants of Bacillus subtilis.
    Mol Gen Genet. 1979 Feb 16;170(1):67-74 PMID: 108515
  10. Catabolite repression-resistant mutants of Bacillus subtilis.
    Can J Microbiol. 1979 Nov;25(11):1283-7 PMID: 120218
  11. Use of a lacZ fusion to study the role of the spoO genes of Bacillus subtilis in developmental regulation.
    Cell. 1983 Nov;35(1):275-83 PMID: 6414720
  12. 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 PMID: 8497199
  13. Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon.
    J Bacteriol. 1993 Aug;175(15):4605-14 PMID: 8335620
  14. Alanine dehydrogenase (ald) is required for normal sporulation in Bacillus subtilis.
    J Bacteriol. 1993 Nov;175(21):6789-96 PMID: 8226620
  15. Phosphorylation of Spo0A activates its stimulation of in vitro transcription from the Bacillus subtilis spoIIG operon.
    Mol Microbiol. 1993 Aug;9(4):741-9 PMID: 8231806
  16. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis.
    Annu Rev Microbiol. 1993;47:441-65 PMID: 8257105
  17. 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 PMID: 8288522
  18. Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation.
    J Bacteriol. 1994 Apr;176(7):1977-84 PMID: 8144465
  19. A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis.
    EMBO J. 1994 Apr 1;13(7):1566-73 PMID: 8156995
  20. Activation of spo0A transcription by sigma H is necessary for sporulation but not for competence in Bacillus subtilis.
    J Bacteriol. 1994 Jun;176(12):3812-5 PMID: 8206860
  21. Identification of two distinct Bacillus subtilis citrate synthase genes.
    J Bacteriol. 1994 Aug;176(15):4669-79 PMID: 8045898
  22. Transcriptional regulation of Bacillus subtilis citrate synthase genes.
    J Bacteriol. 1994 Aug;176(15):4680-90 PMID: 8045899
  23. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis.
    J Bacteriol. 1994 Sep;176(17):5320-9 PMID: 8071208
  24. 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
  25. 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):176-82 PMID: 8002615
  26. Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis.
    J Bacteriol. 1995 Feb;177(3):861-3 PMID: 7836330
  27. Isolation and mapping of a new suppressor mutation of an early sporulation gene spoOF mutation in Bacillus subtilis.
    Mol Gen Genet. 1983;192(3):330-4 PMID: 6419021
  28. Identification of the transcriptional suppressor sof-1 as an alteration in the spo0A protein.
    J Bacteriol. 1985 Feb;161(2):552-5 PMID: 2981817
  29. Catabolite-resistant sporulation (crsA) mutations in the Bacillus subtilis RNA polymerase sigma 43 gene (rpoD) can suppress and be suppressed by mutations in spo0 genes.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8124-8 PMID: 3934667
  30. Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis.
    J Bacteriol. 1987 May;169(5):2223-30 PMID: 2437099
  31. 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):2560-7 PMID: 3131303
  32. 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
  33. 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
  34. Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis.
    J Bacteriol. 1989 Aug;171(8):4121-9 PMID: 2502532
  35. The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein.
    EMBO J. 1989 May;8(5):1615-21 PMID: 2504584
  36. 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):6187-96 PMID: 2509430
  37. 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):8457-61 PMID: 2554317
  38. New suppressor mutation sur0B of spo0B and spo0F mutations in Bacillus subtilis.
    J Gen Microbiol. 1988 Dec;134(12):3249-57 PMID: 3151993
  39. Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9109-13 PMID: 2512576
  40. 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 PMID: 2104615
  41. 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
  42. Dissection of the expression signals of the spoA gene of Bacillus subtilis: glucose represses sporulation-specific expression.
    J Gen Microbiol. 1989 May;135(5):1335-45 PMID: 2516118
  43. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene.
    Proc Natl Acad Sci U S A. 1990 Mar;87(5):1801-5 PMID: 2106683
  44. A novel Bacillus subtilis gene involved in negative control of sporulation and degradative-enzyme production.
    J Bacteriol. 1990 Apr;172(4):1783-90 PMID: 2108124
  45. A forespore checkpoint for mother cell gene expression during development in B. subtilis.
    Cell. 1990 Jul 27;62(2):239-50 PMID: 2115401
  46. Structural alterations in the Bacillus subtilis Spo0A regulatory protein which suppress mutations at several spo0 loci.
    J Bacteriol. 1990 Sep;172(9):5011-9 PMID: 2118505
  47. Novel mutations that alter the regulation of sporulation in Bacillus subtilis. Evidence that phosphorylation of regulatory protein SpoOA controls the initiation of sporulation.
    J Mol Biol. 1990 Oct 5;215(3):359-72 PMID: 2121995
  48. Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor.
    J Bacteriol. 1991 Jan;173(2):521-9 PMID: 1898930
  49. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay.
    Cell. 1991 Feb 8;64(3):545-52 PMID: 1846779
  50. Differential regulation of spo0A transcription in Bacillus subtilis: glucose represses promoter switching at the initiation of sporulation.
    J Bacteriol. 1991 Apr;173(8):2625-32 PMID: 1901572
  51. 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):4533-7 PMID: 1903544
  52. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis.
    Nature. 1992 Feb 13;355(6361):601-4 PMID: 1538747
  53. Spo0A controls the sigma A-dependent activation of Bacillus subtilis sporulation-specific transcription unit spoIIE.
    J Bacteriol. 1992 Apr;174(8):2648-58 PMID: 1556084
  54. 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
  55. Role of the Bacillus subtilis gsiA gene in regulation of early sporulation gene expression.
    J Bacteriol. 1992 Jul;174(13):4374-83 PMID: 1624431
  56. 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):8808-12 PMID: 1528896
  57. Spo0A activates and represses its own synthesis by binding at its dual promoters.
    Biochimie. 1992 Jul-Aug;74(7-8):619-26 PMID: 1391039
  58. Suppressors of a spo0A missense mutation and their effects on sporulation in Bacillus subtilis.
    Biochimie. 1992 Jul-Aug;74(7-8):679-88 PMID: 1391047
  59. Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor.
    Genes Dev. 1993 Feb;7(2):283-94 PMID: 8436298
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-03-28
Pages
2845-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC42315
Subset
IM
Grants
NIGMS NIH HHS · GM36718 · United States
NIGMS NIH HHS · GM41934 · 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]