Home LiteratureArticle Details
PMID: 9696769 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Fnr, NarP, and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro.

Journal of bacteriology ·Vol. 180 ·No. 16 ·1998-08-00 ·Pages 4192-8

Darwin AJ, Ziegelhoffer EC, Kiley PJ, Stewart V

Abstract

The expression of several Escherichia coli operons is activated by the Fnr protein during anaerobic growth and is further controlled in response to nitrate and nitrite by the homologous response regulators, NarL and NarP. Among these operons, the napF operon, encoding a periplasmic nitrate reductase, has unique features with respect to its Fnr-, NarL-, and NarP-dependent regulation. First, the Fnr-binding site is unusually located compared to the control regions of most other Fnr-activated operons, suggesting different Fnr-RNA polymerase contacts during transcriptional activation. Second, nitrate and nitrite activation is solely dependent on NarP but is antagonized by the NarL protein. In this study, we used DNase I footprint analysis to confirm our previous assignment of the unusual location of the Fnr-binding site in the napF control region. In addition, the in vivo effects of Fnr-positive control mutations on napF operon expression indicate that the napF promoter is atypical with respect to Fnr-mediated activation. The transcriptional regulation of napF was successfully reproduced in vitro by using a supercoiled plasmid template and purified Fnr, NarL, and NarP proteins. These in vitro transcription experiments demonstrate that, in the presence of Fnr, the NarP protein causes efficient transcription activation whereas the NarL protein does not. This suggests that Fnr and NarP may act synergistically to activate napF operon expression. As observed in vivo, this activation by Fnr and NarP is antagonized by the addition of NarL in vitro.

MeSH Terms
Bacterial Proteins/metabolism DNA-Binding Proteins/metabolism Escherichia coli/genetics Escherichia coli Proteins Gene Expression Regulation, Bacterial Gene Expression Regulation, Enzymologic Iron-Sulfur Proteins/metabolism Nitrate Reductase Nitrate Reductases/genetics Operon Promoter Regions, Genetic Transcription, Genetic
Chemicals
Bacterial Proteins DNA-Binding Proteins Escherichia coli Proteins FNR protein, E coli Iron-Sulfur Proteins narP protein, E coli NarL protein, E coli Nitrate Reductases Nitrate Reductase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Darwin A J
Section of Microbiology, Cornell University, Ithaca, New York 14853, USA.
Ziegelhoffer E C
Kiley P J
Stewart V
References (26)
26 references, click to expand
  1. Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12.
    J Bacteriol. 1988 Apr;170(4):1589-97 PMID: 2832370
  2. Transcription activation at class I FNR-dependent promoters: identification of the activating surface of FNR and the corresponding contact site in the C-terminal domain of the RNA polymerase alpha subunit.
    Nucleic Acids Res. 1997 Oct 15;25(20):4028-34 PMID: 9321653
  3. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression.
    Genes Dev. 1989 Sep;3(9):1462-71 PMID: 2691330
  4. Substitution of 2 base pairs (1 base pair per DNA half-site) within the Escherichia coli lac promoter DNA site for catabolite gene activator protein places the lac promoter in the FNR regulon.
    J Biol Chem. 1990 Jul 25;265(21):12400-3 PMID: 2165061
  5. Stringent spacing requirements for transcription activation by CRP.
    Cell. 1990 Aug 24;62(4):733-43 PMID: 2167178
  6. The role of two surface exposed loops in transcription activation by the Escherichia coli CRP and FNR proteins.
    Nucleic Acids Res. 1991 Dec 25;19(24):6705-12 PMID: 1762901
  7. Localization of upstream sequence elements required for nitrate and anaerobic induction of fdn (formate dehydrogenase-N) operon expression in Escherichia coli K-12.
    J Bacteriol. 1992 Aug;174(15):4935-42 PMID: 1629153
  8. Upstream sequence elements required for NarL-mediated activation of transcription from the narGHJI promoter of Escherichia coli.
    J Biol Chem. 1992 Jul 15;267(20):14122-8 PMID: 1629213
  9. Identification of the regulatory sequence of anaerobically expressed locus aeg-46.5.
    J Bacteriol. 1993 Feb;175(4):1165-72 PMID: 8432709
  10. Definition of nitrite and nitrate response elements at the anaerobically inducible Escherichia coli nirB promoter: interactions between FNR and NarL.
    Mol Microbiol. 1993 Jan;7(1):151-7 PMID: 8437517
  11. Synergistic activation of transcription by Escherichia coli cAMP receptor protein.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3083-7 PMID: 7681995
  12. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12.
    J Bacteriol. 1993 Jun;175(11):3259-68 PMID: 8501030
  13. The activity of the Escherichia coli transcription factor FNR is regulated by a change in oligomeric state.
    Genes Dev. 1993 Oct;7(10):1993-2005 PMID: 8406003
  14. Location and orientation of an activating region in the Escherichia coli transcription factor, FNR.
    Mol Microbiol. 1994 Jan;11(2):383-90 PMID: 8170400
  15. In vitro interaction of nitrate-responsive regulatory protein NarL with DNA target sequences in the fdnG, narG, narK and frdA operon control regions of Escherichia coli K-12.
    J Mol Biol. 1994 Aug 12;241(2):150-65 PMID: 8057356
  16. Transcription activation by the Escherichia coli cyclic AMP receptor protein. Receptors bound in tandem at promoters can interact synergistically.
    J Mol Biol. 1994 Aug 19;241(3):341-52 PMID: 7520503
  17. Synergistic activation of transcription by bacteriophage lambda cI protein and E. coli cAMP receptor protein.
    Science. 1994 Sep 23;265(5180):1863-6 PMID: 8091212
  18. In vitro analysis of a constitutively active mutant form of the Escherichia coli global transcription factor FNR.
    J Mol Biol. 1995 Jan 27;245(4):351-61 PMID: 7837268
  19. Expression of the narX, narL, narP, and narQ genes of Escherichia coli K-12: regulation of the regulators.
    J Bacteriol. 1995 Jul;177(13):3865-9 PMID: 7601854
  20. Nitrate and nitrite regulation of the Fnr-dependent aeg-46.5 promoter of Escherichia coli K-12 is mediated by competition between homologous response regulators (NarL and NarP) for a common DNA-binding site.
    J Mol Biol. 1995 Aug 4;251(1):15-29 PMID: 7643383
  21. Spacing requirements for transcription activation by Escherichia coli FNR protein.
    J Bacteriol. 1995 Dec;177(23):6704-10 PMID: 7592457
  22. Analysis of nitrate regulatory protein NarL-binding sites in the fdnG and narG operon control regions of Escherichia coli K-12.
    Mol Microbiol. 1996 May;20(3):621-32 PMID: 8736541
  23. On the role of the multiple regulatory elements involved in the activation of the Escherichia coli malEp promoter.
    J Mol Biol. 1996 Dec 20;264(5):852-62 PMID: 9000616
  24. Transcription activation at class II CAP-dependent promoters.
    Mol Microbiol. 1997 Mar;23(5):853-9 PMID: 9076723
  25. Differential regulation by the homologous response regulators NarL and NarP of Escherichia coli K-12 depends on DNA binding site arrangement.
    Mol Microbiol. 1997 Aug;25(3):583-95 PMID: 9302020
  26. Activation of the lac operon of Escherichia coli by a mutant FNR protein.
    Mol Microbiol. 1987 Jul;1(1):53-8 PMID: 2838728
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1998-08-00
Pages
4192-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC107417
Subset
IM
Grants
NIGMS NIH HHS · T32 GM007215 · United States
NIGMS NIH HHS · R01 GM036877 · United States
NIGMS NIH HHS · R01 GM045844 · United States
NIGMS NIH HHS · GM45844 · United States
NIGMS NIH HHS · GM07215 · United States
NIGMS NIH HHS · GM36877 · 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]