Home LiteratureArticle Details
PMID: 11325953 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Two ResD-controlled promoters regulate ctaA expression in Bacillus subtilis.

Journal of bacteriology ·Vol. 183 ·No. 10 ·2001-05-00 ·Pages 3237-46

Paul S, Zhang X, Hulett FM

Abstract

The Bacillus subtilis ResDE two-component system plays a positive role in global regulation of genes involved in aerobic and anaerobic respiration. ctaA is one of the several genes involved in aerobic respiration that requires ResD for in vivo expression. The ctaAB-divergent promoter regulatory region has three ResD binding sites; A1, A2, and A3. The A2 site is essential for in vivo promoter activity, while binding sites A2 and A3 are required for full ctaA promoter activity. In this study, we demonstrate the role of ResD~P in the activation of the ctaA promoter using an in vitro transcription system. The results indicate that the ctaA promoter (binding sites A2 and A3) has two transcriptional start sites. Binding site A2 was sufficient for weak transcription of the upstream promoter (Pv) by Esigma(A), transcription which was enhanced approximately 1.5-fold by ResD and 5-fold by ResD~P. The downstream promoter (Ps) required both binding sites A2 and A3 and was not transcribed by Esigma(A) with or without ResD~P. RNA polymerase (RNAP) isolated from B. subtilis when cells were at the end of exponential growth (T(0)) or 3, 4, or 5 h into the stationary phase (T(3), T(4), or T( 5), respectively) was used in in vitro transcription assays. Maximal transcription from Ps required T(4) RNAP plus ResD~P. RNAP isolated from a spo0A or a sigE mutant strain was not capable of Ps transcription. Comparison of the Ps promoter sequence with the SigE binding consensus suggests that the ctaA Ps promoter may be a SigE promoter. The collective data from ResD footprinting, in vivo promoter deletion analysis, and in vitro transcription assays suggest that ctaA is transcribed during late exponential to early stationary phases of growth from the Pv promoter, which requires ResD binding site A2, Esigma(A), and ResD~P, and during later stationary phase from Ps, which requires binding sites A2 and A3, ResD~P, and Esigma(E) or a sigma factor whose transcription is dependent on SigE.

MeSH Terms
Aerobiosis Bacillus subtilis/genetics,growth & development,metabolism Bacterial Proteins/genetics,metabolism Base Sequence Cytochrome b Group/genetics,metabolism DNA-Binding Proteins DNA-Directed RNA Polymerases/metabolism Gene Expression Regulation, Bacterial Histidine Kinase Membrane Proteins/genetics,metabolism Molecular Sequence Data Phosphorylation Promoter Regions, Genetic/genetics Protein Kinases/genetics,metabolism Sigma Factor/metabolism Signal Transduction Transcription Factors Transcription, Genetic
Chemicals
Bacterial Proteins CtaA protein, bacteria Cytochrome b Group DNA-Binding Proteins Membrane Proteins ResD protein, Bacillus subtilis Sigma Factor Transcription Factors Protein Kinases Histidine Kinase DNA-Directed RNA Polymerases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Paul S
Laboratory for Molecular Biology, Department of Biological Sciences, University of Illinois at Chicago, 900 S. Ashland Ave., Chicago, IL 60607, USA.
Zhang X
Hulett F M
References (30)
30 references, click to expand
  1. Genes required for cytochrome c synthesis in Bacillus subtilis.
    Mol Microbiol. 2000 May;36(3):638-50 PMID: 10844653
  2. Separate contributions of UhpA and CAP to activation of transcription of the uhpT promoter of Escherichia coli.
    J Mol Biol. 1999 Oct 8;292(5):973-86 PMID: 10512697
  3. ResD signal transduction regulator of aerobic respiration in Bacillus subtilis: ctaA promoter regulation.
    Mol Microbiol. 2000 Sep;37(5):1208-19 PMID: 10972837
  4. Mutations conferring amino acid residue substitutions in the carboxy-terminal domain of RNA polymerase alpha can suppress clpX and clpP with respect to developmentally regulated transcription in Bacillus subtilis.
    Mol Microbiol. 2000 Aug;37(4):869-84 PMID: 10972808
  5. The ClpX protein of Bacillus subtilis indirectly influences RNA polymerase holoenzyme composition and directly stimulates sigma-dependent transcription.
    Mol Microbiol. 2000 Aug;37(4):885-97 PMID: 10972809
  6. Terminal oxidases of Bacillus subtilis strain 168: one quinol oxidase, cytochrome aa(3) or cytochrome bd, is required for aerobic growth.
    J Bacteriol. 2000 Dec;182(23):6557-64 PMID: 11073895
  7. Regulation of sigma factor activity during Bacillus subtilis development.
    Curr Opin Microbiol. 2000 Dec;3(6):553-60 PMID: 11121773
  8. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  9. The stability of messenger ribonucleic acid during sporulation in Bacillus subtilis.
    J Biol Chem. 1971 May 25;246(10):3189-95 PMID: 4995746
  10. Loss of the sigma activity of RNA polymerase of Bacillus subtilis during sporulation.
    Proc Natl Acad Sci U S A. 1973 Jun;70(6):1865-9 PMID: 4198276
  11. An immunological assay for the sigma subunit of RNA polymerase in extracts of vegetative and sporulating Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1974 Jul;71(7):2872-6 PMID: 4211798
  12. Structure and expression of the cytochrome aa3 regulatory gene ctaA of Bacillus subtilis.
    J Bacteriol. 1989 Sep;171(9):4979-86 PMID: 2549007
  13. The Bacillus subtilis cytochrome-c oxidase. Variations on a conserved protein theme.
    Eur J Biochem. 1991 Jan 30;195(2):517-25 PMID: 1847686
  14. Separate promoters direct expression of phoAIII, a member of the Bacillus subtilis alkaline phosphatase multigene family, during phosphate starvation and sporulation.
    Mol Microbiol. 1991 Sep;5(9):2181-90 PMID: 1766385
  15. The sigma 70 family: sequence conservation and evolutionary relationships.
    J Bacteriol. 1992 Jun;174(12):3843-9 PMID: 1597408
  16. Bacillus subtilis CtaA is a heme-containing membrane protein involved in heme A biosynthesis.
    J Bacteriol. 1994 Nov;176(21):6663-71 PMID: 7961419
  17. Bacillus subtilis CtaA and CtaB function in haem A biosynthesis.
    Mol Microbiol. 1993 Oct;10(1):193-201 PMID: 7968515
  18. Regulators of aerobic and anaerobic respiration in Bacillus subtilis.
    J Bacteriol. 1996 Mar;178(5):1374-85 PMID: 8631715
  19. Basic mechanisms of transcript elongation and its regulation.
    Annu Rev Biochem. 1997;66:117-72 PMID: 9242904
  20. Bacillus subtilis PhoP binds to the phoB tandem promoter exclusively within the phosphate starvation-inducible promoter.
    J Bacteriol. 1997 Oct;179(20):6302-10 PMID: 9335276
  21. Regulation of Bacillus subtilis sigmaH (spo0H) and AbrB in response to changes in external pH.
    J Bacteriol. 1997 Nov;179(21):6778-87 PMID: 9352930
  22. The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
    Nature. 1997 Nov 20;390(6657):249-56 PMID: 9384377
  23. Adaptation of Bacillus subtilis to oxygen limitation.
    FEMS Microbiol Lett. 1997 Dec 1;157(1):1-7 PMID: 9418235
  24. PhoP-P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP-P activator sites within the coding region stimulate transcription in vitro.
    Mol Microbiol. 1998 Jun;28(6):1187-97 PMID: 9680208
  25. Role of Pho-P in transcriptional regulation of genes involved in cell wall anionic polymer biosynthesis in Bacillus subtilis.
    J Bacteriol. 1998 Aug;180(15):4007-10 PMID: 9683503
  26. Catabolite regulation of the Bacillus subtilis ctaBCDEF gene cluster.
    J Bacteriol. 1998 Dec;180(23):6154-63 PMID: 9829923
  27. Role of lon and ClpX in the post-translational regulation of a sigma subunit of RNA polymerase required for cellular differentiation in Bacillus subtilis.
    Mol Microbiol. 1999 Jul;33(2):415-28 PMID: 10411757
  28. Sigma factor displacement from RNA polymerase during Bacillus subtilis sporulation.
    J Bacteriol. 1999 Aug;181(16):4969-77 PMID: 10438769
  29. RNA polymerase unveiled.
    Cell. 1999 Sep 17;98(6):687-90 PMID: 10499791
  30. Interaction of ResD with regulatory regions of anaerobically induced genes in Bacillus subtilis.
    Mol Microbiol. 2000 Sep;37(5):1198-207 PMID: 10972836
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2001-05-00
Pages
3237-46
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC95225
Subset
IM
Grants
NIGMS NIH HHS · R01 GM033471 · United States
NIGMS NIH HHS · R01 GM033471-16 · United States
NIGMS NIH HHS · GM33471 · 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: product@genelibs.com