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J Bacteriol. Jun 1993; 175(11): 3259–3268.
PMCID: PMC204722

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.

Abstract

Two sensor proteins, NarX and NarQ, mediate nitrate regulation of anaerobic respiratory gene expression. Either of these sensors is sufficient to signal the presence of nitrate to the response regulator protein, NarL, a transcriptional activator and repressor. Two observations suggested the existence of a second response regulator that is also involved in nitrate regulation. First, narL null mutants retain residual nitrate induction of fdnG operon expression; this residual induction is absent in narX narQ double-null strains. Second, nitrate induction of aeg-46.5 operon expression is substantially enhanced in narL null strains (M.H. Choe and W.S. Reznikoff, J. Bacteriol. 173:6139-6146, 1991). We found that this nitrate induction requires either the NarX or the NarQ protein, consistent with the existence of a second response regulator. We designate this second regulator NarP. We isolated insertion mutants that are defective in aeg-46.5 operon expression. These insertions are in the narP gene, which encodes a response regulator that is 44% identical to the NarL protein. Null alleles of narP abolished aeg-46.5 induction and also eliminated the residual NarL-independent nitrate induction of fdnG operon expression. Both the NarX and NarQ proteins communicate with both the NarP and NarL proteins. We found that the primary signal for NarP-dependent aeg-46.5 operon induction is nitrite rather than nitrate. By contrast, nitrite is a relatively weak signal for NarL-dependent induction. In narX null strains, nitrate was an efficient signal for NarL-dependent induction, and this induction required the NarQ protein. We conclude that, in wild-type strains, the NarQ protein communicates the presence of nitrite to both the NarP and NarL proteins and that the NarX protein inhibits this communication with the NarL protein.

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Selected References

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  • Berg BL, Li J, Heider J, Stewart V. Nitrate-inducible formate dehydrogenase in Escherichia coli K-12. I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J Biol Chem. 1991 Nov 25;266(33):22380–22385. [PubMed]
  • Berg BL, Stewart V. Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12. Genetics. 1990 Aug;125(4):691–702. [PMC free article] [PubMed]
  • Birkenbihl RP, Vielmetter W. Complete maps of IS1, IS2, IS3, IS4, IS5, IS30 and IS150 locations in Escherichia coli K12. Mol Gen Genet. 1989 Dec;220(1):147–153. [PubMed]
  • Castilho BA, Olfson P, Casadaban MJ. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. [PMC free article] [PubMed]
  • Chiang RC, Cavicchioli R, Gunsalus RP. Identification and characterization of narQ, a second nitrate sensor for nitrate-dependent gene regulation in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1913–1923. [PubMed]
  • Choe M, Reznikoff WS. Anaerobically expressed Escherichia coli genes identified by operon fusion techniques. J Bacteriol. 1991 Oct;173(19):6139–6146. [PMC free article] [PubMed]
  • Choe M, Reznikoff WS. Identification of the regulatory sequence of anaerobically expressed locus aeg-46.5. J Bacteriol. 1993 Feb;175(4):1165–1172. [PMC free article] [PubMed]
  • Collins LA, Egan SM, Stewart V. Mutational analysis reveals functional similarity between NARX, a nitrate sensor in Escherichia coli K-12, and the methyl-accepting chemotaxis proteins. J Bacteriol. 1992 Jun;174(11):3667–3675. [PMC free article] [PubMed]
  • DeMoss JA, Hsu PY. NarK enhances nitrate uptake and nitrite excretion in Escherichia coli. J Bacteriol. 1991 Jun;173(11):3303–3310. [PMC free article] [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Dong XR, Li SF, DeMoss JA. 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):14122–14128. [PubMed]
  • Egan SM, Stewart V. Nitrate regulation of anaerobic respiratory gene expression in narX deletion mutants of Escherichia coli K-12. J Bacteriol. 1990 Sep;172(9):5020–5029. [PMC free article] [PubMed]
  • Egan SM, Stewart V. Mutational analysis of nitrate regulatory gene narL in Escherichia coli K-12. J Bacteriol. 1991 Jul;173(14):4424–4432. [PMC free article] [PubMed]
  • Erpel T, Hwang P, Craik CS, Fletterick RJ, McGrath ME. Physical map location of the new Escherichia coli gene eco, encoding the serine protease inhibitor ecotin. J Bacteriol. 1992 Mar;174(5):1704–1704. [PMC free article] [PubMed]
  • Iuchi S, Lin EC. The narL gene product activates the nitrate reductase operon and represses the fumarate reductase and trimethylamine N-oxide reductase operons in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3901–3905. [PMC free article] [PubMed]
  • Kahn D, Ditta G. Modular structure of FixJ: homology of the transcriptional activator domain with the -35 binding domain of sigma factors. Mol Microbiol. 1991 Apr;5(4):987–997. [PubMed]
  • Kalman LV, Gunsalus RP. The frdR gene of Escherichia coli globally regulates several operons involved in anaerobic growth in response to nitrate. J Bacteriol. 1988 Feb;170(2):623–629. [PMC free article] [PubMed]
  • Kleckner N, Bender J, Gottesman S. Uses of transposons with emphasis on Tn10. Methods Enzymol. 1991;204:139–180. [PubMed]
  • Kohara Y, Akiyama K, Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. [PubMed]
  • Li J, Stewart V. 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):4935–4942. [PMC free article] [PubMed]
  • Muramatsu S, Kato M, Kohara Y, Mizuno T. Insertion sequence IS5 contains a sharply curved DNA structure at its terminus. Mol Gen Genet. 1988 Nov;214(3):433–438. [PubMed]
  • Neidhardt FC, Bloch PL, Smith DF. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. [PMC free article] [PubMed]
  • Page L, Griffiths L, Cole JA. Different physiological roles of two independent pathways for nitrite reduction to ammonia by enteric bacteria. Arch Microbiol. 1990;154(4):349–354. [PubMed]
  • Parkinson JS, Kofoid EC. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. [PubMed]
  • Rabin RS, Collins LA, Stewart V. In vivo requirement of integration host factor for nar (nitrate reductase) operon expression in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8701–8705. [PMC free article] [PubMed]
  • Rabin RS, Stewart V. Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8419–8423. [PMC free article] [PubMed]
  • Russo FD, Silhavy TJ. EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol. 1991 Dec 5;222(3):567–580. [PubMed]
  • Singer M, Baker TA, Schnitzler G, Deischel SM, Goel M, Dove W, Jaacks KJ, Grossman AD, Erickson JW, Gross CA. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. [PMC free article] [PubMed]
  • Slauch JM, Silhavy TJ. Genetic analysis of the switch that controls porin gene expression in Escherichia coli K-12. J Mol Biol. 1989 Nov 20;210(2):281–292. [PubMed]
  • Slauch JM, Silhavy TJ. cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J Bacteriol. 1991 Jul;173(13):4039–4048. [PMC free article] [PubMed]
  • Spiro S, Guest JR. FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev. 1990 Aug;6(4):399–428. [PubMed]
  • Stewart GS, Lubinsky-Mink S, Jackson CG, Cassel A, Kuhn J. pHG165: a pBR322 copy number derivative of pUC8 for cloning and expression. Plasmid. 1986 May;15(3):172–181. [PubMed]
  • Stewart V. Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol. 1982 Sep;151(3):1320–1325. [PMC free article] [PubMed]
  • Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev. 1988 Jun;52(2):190–232. [PMC free article] [PubMed]
  • Stewart V, Berg BL. Influence of nar (nitrate reductase) genes on nitrate inhibition of formate-hydrogen lyase and fumarate reductase gene expression in Escherichia coli K-12. J Bacteriol. 1988 Oct;170(10):4437–4444. [PMC free article] [PubMed]
  • Stewart V, Parales J., Jr 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):1589–1597. [PMC free article] [PubMed]
  • Stout V, Torres-Cabassa A, Maurizi MR, Gutnick D, Gottesman S. RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J Bacteriol. 1991 Mar;173(5):1738–1747. [PMC free article] [PubMed]
  • Tyson KL, Bell AI, Cole JA, Busby SJ. 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):151–157. [PubMed]

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