• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Mar 1990; 87(6): 2369–2373.
PMCID: PMC53688

FlbD of Caulobacter crescentus is a homologue of the NtrC (NRI) protein and activates sigma 54-dependent flagellar gene promoters.

Abstract

The periodic transcription of flagellar genes in the Caulobacter crescentus cell cycle is controlled, in part, by their organization in a regulatory hierarchy. The flbG (hook operon), flaN, and flagellin gene operons, which are at the lowest levels of the hierarchy and expressed late in the cell cycle, contain Ntr-like promoters. We report that flbD, one of the early genes required in trans for expression of these operons, codes for a 52-kDa protein homologous to the transcriptional activators NtrC (NRI), NifA, DctD, HydG, and XylR. Our results show that in Escherichia coli flbD partially complements glnG (ntrC) mutations and stimulates transcription of the C. crescentus sigma 54 RNA polymerase-dependent flbG gene. Additionally, the sequence predicts that FlbD protein, along with NtrC, DctD, and HydG proteins, is structurally related at the amino-terminal domain to a larger family of response regulators that mediate cellular responses to environmental stimuli. FlbD may be a singular member of this large protein family in that its function is tied to an internal cell-cycle signal. FlbD is also unusual in that its amino-terminal domain contains only one of the three residues conserved in previously described members of this family of response regulators.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.4M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Shapiro L. Generation of polarity during Caulobacter cell differentiation. Annu Rev Cell Biol. 1985;1:173–207. [PubMed]
  • Newton A, Ohta N, Ramakrishnan G, Mullin D, Raymond G. Genetic switching in the flagellar gene hierarchy of Caulobacter requires negative as well as positive regulation of transcription. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6651–6655. [PMC free article] [PubMed]
  • Mullin D, Minnich S, Chen LS, Newton A. A set of positively regulated flagellar gene promoters in Caulobacter crescentus with sequence homology to the nif gene promoters of Klebsiella pneumoniae. J Mol Biol. 1987 Jun 20;195(4):939–943. [PubMed]
  • Ninfa AJ, Mullin DA, Ramakrishnan G, Newton A. Escherichia coli sigma 54 RNA polymerase recognizes Caulobacter crescentus flbG and flaN flagellar gene promoters in vitro. J Bacteriol. 1989 Jan;171(1):383–391. [PMC free article] [PubMed]
  • Minnich SA, Newton A. Promoter mapping and cell cycle regulation of flagellin gene transcription in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1142–1146. [PMC free article] [PubMed]
  • Hirschman J, Wong PK, Sei K, Keener J, Kustu S. Products of nitrogen regulatory genes ntrA and ntrC of enteric bacteria activate glnA transcription in vitro: evidence that the ntrA product is a sigma factor. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7525–7529. [PMC free article] [PubMed]
  • Hunt TP, Magasanik B. Transcription of glnA by purified Escherichia coli components: core RNA polymerase and the products of glnF, glnG, and glnL. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8453–8457. [PMC free article] [PubMed]
  • Mullin DA, Newton A. Ntr-like promoters and upstream regulatory sequence ftr are required for transcription of a developmentally regulated Caulobacter crescentus flagellar gene. J Bacteriol. 1989 Jun;171(6):3218–3227. [PMC free article] [PubMed]
  • Kustu S, Santero E, Keener J, Popham D, Weiss D. Expression of sigma 54 (ntrA)-dependent genes is probably united by a common mechanism. Microbiol Rev. 1989 Sep;53(3):367–376. [PMC free article] [PubMed]
  • Ronson CW, Nixon BT, Ausubel FM. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell. 1987 Jun 5;49(5):579–581. [PubMed]
  • Bourret RB, Hess JF, Borkovich KA, Pakula AA, Simon MI. Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. J Biol Chem. 1989 May 5;264(13):7085–7088. [PubMed]
  • Stock JB, Ninfa AJ, Stock AM. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. [PMC free article] [PubMed]
  • Ninfa AJ, Magasanik B. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5909–5913. [PMC free article] [PubMed]
  • Keener J, Kustu S. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci U S A. 1988 Jul;85(14):4976–4980. [PMC free article] [PubMed]
  • Reitzer LJ, Magasanik B. Transcription of glnA in E. coli is stimulated by activator bound to sites far from the promoter. Cell. 1986 Jun 20;45(6):785–792. [PubMed]
  • Drummond M, Whitty P, Wootton J. Sequence and domain relationships of ntrC and nifA from Klebsiella pneumoniae: homologies to other regulatory proteins. EMBO J. 1986 Feb;5(2):441–447. [PMC free article] [PubMed]
  • Ronson CW, Astwood PM, Nixon BT, Ausubel FM. Deduced products of C4-dicarboxylate transport regulatory genes of Rhizobium leguminosarum are homologous to nitrogen regulatory gene products. Nucleic Acids Res. 1987 Oct 12;15(19):7921–7934. [PMC free article] [PubMed]
  • Stoker K, Reijnders WN, Oltmann LF, Stouthamer AH. Initial cloning and sequencing of hydHG, an operon homologous to ntrBC and regulating the labile hydrogenase activity in Escherichia coli K-12. J Bacteriol. 1989 Aug;171(8):4448–4456. [PMC free article] [PubMed]
  • Inouye S, Nakazawa A, Nakazawa T. Nucleotide sequence of the regulatory gene xylR of the TOL plasmid from Pseudomonas putida. Gene. 1988 Jun 30;66(2):301–306. [PubMed]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [PubMed]
  • Ohta N, Swanson E, Ely B, Newton A. Physical mapping and complementation analysis of transposon Tn5 mutations in Caulobacter crescentus: organization of transcriptional units in the hook gene cluster. J Bacteriol. 1984 Jun;158(3):897–904. [PMC free article] [PubMed]
  • Backman K, Chen YM, Magasanik B. Physical and genetic characterization of the glnA--glnG region of the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3743–3747. [PMC free article] [PubMed]
  • Ow DW, Ausubel FM. Regulation of nitrogen metabolism genes by nifA gene product in Klebsiella pneumoniae. Nature. 1983 Jan 27;301(5898):307–313. [PubMed]
  • Bender RA, Janssen KA, Resnick AD, Blumenberg M, Foor F, Magasanik B. Biochemical parameters of glutamine synthetase from Klebsiella aerogenes. J Bacteriol. 1977 Feb;129(2):1001–1009. [PMC free article] [PubMed]
  • Postle K, Reznikoff WS. Identification of the Escherichia coli tonB gene product in minicells containing tonB hybrid plasmids. J Mol Biol. 1979 Jul 5;131(3):619–636. [PubMed]
  • Ross CM, Winkler ME. Structure of the Caulobacter crescentus trpFBA operon. J Bacteriol. 1988 Feb;170(2):757–768. [PMC free article] [PubMed]
  • Hahnenberger KM, Shapiro L. Organization and temporal expression of a flagellar basal body gene in Caulobacter crescentus. J Bacteriol. 1988 Sep;170(9):4119–4124. [PMC free article] [PubMed]
  • Kaplan JB, Dingwall A, Bryan R, Champer R, Shapiro L. Temporal regulation and overlap organization of two Caulobacter flagellar genes. J Mol Biol. 1989 Jan 5;205(1):71–83. [PubMed]
  • Lipman DJ, Pearson WR. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. [PubMed]
  • Stock AM, Mottonen JM, Stock JB, Schutt CE. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature. 1989 Feb 23;337(6209):745–749. [PubMed]
  • Pabo CO, Sauer RT. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. [PubMed]
  • Dodd IB, Egan JB. Systematic method for the detection of potential lambda Cro-like DNA-binding regions in proteins. J Mol Biol. 1987 Apr 5;194(3):557–564. [PubMed]
  • Contreras A, Drummond M. The effect on the function of the transcriptional activator NtrC from Klebsiella pneumoniae of mutations in the DNA-recognition helix. Nucleic Acids Res. 1988 May 11;16(9):4025–4039. [PMC free article] [PubMed]
  • Morett E, Cannon W, Buck M. The DNA-binding domain of the transcriptional activator protein NifA resides in its carboxy terminus, recognises the upstream activator sequences of nif promoters and can be separated from the positive control function of NifA. Nucleic Acids Res. 1988 Dec 23;16(24):11469–11488. [PMC free article] [PubMed]
  • Inouye S, Inouye M. Up-promoter mutations in the lpp gene of Escherichia coli. Nucleic Acids Res. 1985 May 10;13(9):3101–3110. [PMC free article] [PubMed]
  • Ditta G, Stanfield S, Corbin D, Helinski DR. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. [PMC free article] [PubMed]
  • Sheffery M, Newton A. Regulation of periodic protein synthesis in the cell cycle: control of initiation and termination of flagellar gene expression. Cell. 1981 Apr;24(1):49–57. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

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...