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Antonie van Leeuwenhoek

, Volume 66, Issue 1–3, pp 23–36 | Cite as

The FNR family of transcriptional regulators

  • Stephen Spiro
Research Articles

Abstract

Homologues of the transcriptional regulator FNR fromEscherichia coli have been identified in a variety of taxonomically diverse bacterial species. Despite being structurally very similar, members of the FNR family have disparate regulatory roles. Those fromShewanella putrefaciens, Pseudomonas aeruginosa, Pseudomonas stutzeri andRhodopseudomonas palustris are functionally similar to FNR in that they regulate anaerobic respiration or carbon metabolism. Four rhizobial proteins (fromRhizobium meliloti, R. leguminosarum, B. japonicum andAzorhizobium caulinodans) are involved in the regulation of nitrogen fixation; a fifth (fromRhizobium strain IC3342) has unknown function. Two proteins from mammalian pathogens (Actinobacillus pleuropneumoniae andBordetella pertussis) may be involved in the regulation of toxin expression. The FNR protein ofVibrio fischeri regulates bioluminescence, and the function of the one known FNR homologue from a Gram-positive organism (Lactobacillus casei) remains to be elucidated. Some members of this family, like FNR itself, appear to function as sensors of oxygen availability, whereas others do not. The ability to sense and respond to oxygen limitation may be correlated with the presence of cysteine residues which, in the case of FNR, are thought to be involved in oxygen or redox sensing. The mechanism of DNA sequence recognition is probably conserved, or very similar, throughout this family. In a number of other Gram-negative species, there is good indirect evidence for the existence of FNR analogues; these includeAlcaligenes eutrophus, A. denitrificans, A. faecalis, Paracoccus denitrificans and a number ofPseudomonas species.

Key words

Denitrification FNR FNR homologues nitrogen fixation 

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References

  1. Anthamatten D, Scherb B & Hennecke H (1992) Characterization of afixLJ -regulatedBradyrhizobium japonicum gene sharing similarity with theEscherichia coli fnr andRhizobium meliloti fixK Genes. J Bacteriol. 174: 2111–2120Google Scholar
  2. Arai H, Igarashi Y & Kodama T (1991) Anaerobically induced expression of the nitrite reductase cytochromec -551 operon fromPseudomonas aeruginosa. FEBS Lett 280, 351–353Google Scholar
  3. Bannan JD, Moran MJ, MacInnes JI, Soltes GA & Friedman RL (1993) Cloning and characterization ofbtr, aBordetella pertussis gene encoding a FNR-like transcriptional regulator. J. Bacteriol. 175: 7228–7235Google Scholar
  4. Batut J, Daveran-Mingot M-L, David M, Jacobs J, Garnerone AM & Kahn D (1989)fixK, a gene homologous withfnr andcrp fromEscherichiacoli, regulates nitrogen fixation genes both positively and negatively inRhizobium meliloti. EMBO J 8: 1279–1286Google Scholar
  5. Bowie JU, Lüthy R & Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253: 164–170Google Scholar
  6. Cherfils J, Gibrat J-F, Levin J, Batut J & Kahn D (1989) Model-building of Fnr and FixK DNA-binding domains suggests a basis for specific DNA recognition. J. Mol. Recognition 2: 114–121Google Scholar
  7. Colonna-Romano S, Arnold W, Schlüter A, Boistard P, Priefer UB (1990) An Fnr-like protein encoded inRhizobium leguminosarum biovarviciae shows structural and functional homology toRhizobium meliloti FixK. Mol. Gen. Genet. 223: 138–147Google Scholar
  8. Cuypers H & Zumft WG (1992) Regulatory components of the denitrification gene cluster ofPseudomonas stutzeri. pp 188–197 in ‘Pseudomonas molecular biology and biotechnology’ (Eds Galli, E., Silver, S. and Witholt, B.) American Society for Microbiology, Washington, D.C.Google Scholar
  9. Cuypers H & Zumft WG (1993) Anaerobic control of denitrification inPseudomonas stutzeri escapes mutagenesis of anfnr-like gene. J. Bacteriol. 175: 7236–7246Google Scholar
  10. Cuypers H, Viebrock-Sambale A & Zumft WG (1992) NosR, a membrane-boundregulatory componentnecessary for expression of nitrous oxide reductase inPseudomonas stutzeri. J. Bacteriol. 174: 5332–5339Google Scholar
  11. Dispensa M, Thomas C, Kim M-K, Perrotta JA, Gibson J & Harwood CS (1992) Anaerobic growth ofRhodopseudomonas palustris on 4-hydroxybenzoate is dependent on AadR, a member of the cyclic AMP receptor protein family of transcriptional regulators. J. Bacteriol. 174: 5803–5813Google Scholar
  12. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) Version 3.5c. University of Washington, Seattle.Google Scholar
  13. Galimand M, Gamper M, Zimmermann A & Haas D (1991) Positive FNR-like control of anaerobic arginine degradation and nitrate respiration inPseudomonas aeruginosa. J. Bacteriol. 173: 1598–1606Google Scholar
  14. Gilles-Gonzalez M, Ditta G & Helinski DR (1991) A haemoprotein with kinase activity encoded by the oxygen sensor ofRhizobium meliloti. Nature (London) 350: 170–172Google Scholar
  15. Green J, Trageser M, Six S, Unden G & Guest JR (1991) Characterization of the FNR protein ofEscherichia coli, an iron-binding transcriptional regulator. Proc. R. Soc. Lond. B244: 137–144Google Scholar
  16. Green J, Sharrocks AD, MacInnes JI & Guest JR (1992) Purification of HlyX, a potential regulator of haemolysin synthesis, and properties of HlyX:FNR hybrids. Proc. R. Soc. Lond. B248: 79–84Google Scholar
  17. Green J, Sharrocks AD, Green B, Geisow M & Guest JR (1993) Properties of FNR proteins substituted at each of the five cysteine residues. Mol. Microbiol. 8: 61–68Google Scholar
  18. Haas D, Gamper M & Zimmermann A (1992) Anaerobic control inPseudomonas aeruginosa. pp 177–187 in ‘Pseudomonas molecular biology and biotechnology’ (Eds Galli, E., Silver, S. and Witholt, B.) American Society for Microbiology, Washington, D.C.Google Scholar
  19. Hill S (1985) Redox regulation of entericnif expression is independent of thefnr gene product. FEMS Microbiol. Lett. 29: 5–9Google Scholar
  20. Hoitink CWG, Woudt LP, Turenhout JCM, van de Kamp M & Canters GW (1990) Isolation and sequencing of theAlcaligenes denitrificans azurin-encoding gene: comparison with the genes encoding blue copper proteins fromPseudomonas aeruginosa andAlcaligenes faecalis. Gene 90: 15–20Google Scholar
  21. Irvine AS & Guest JR (1993)Lactobacillus casei contains a member of the CRP-FNR family. Nucleic Acids Res. 21: 753Google Scholar
  22. Iuchi S & Lin ECC (1993) Adaptation ofEscherichia coli to redox environments by gene expression. Mol. Microbiol. 9, 9–15Google Scholar
  23. Jüngst A, Wakabayashi S, Matsubara H & Zumft WG (1991) ThenirSTBM region coding for cytochromecd 1-dependent nitrite respiration ofPseudomonas stutzeri consists of a cluster of mono-, di-, and teraheme proteins. FEBS Lett. 279: 205–209Google Scholar
  24. Kaminski PA, Mandon K, Arigoni F, Desnoues N & Elmerich C (1991) Regulation of nitrogen fixation inAzorhizobium caulinodans: identification of afixK-like gene, a positive regulator ofnifA. Mol. Microbiol. 5: 1983–1991Google Scholar
  25. Khosla C & Bailey JE (1989) Characterization of the oxygen-dependent promoter of theVitreoscilla hemoglobin gene inEscherichia coli. J. Bacteriol. 171: 5995–6004Google Scholar
  26. Kita-Tsukamoto K, Oyaizu H, Nanba K & Simidu U (1993) Phylogenetic relationships of marine bacteria, mainly members of the familyVibrionaceae, determined on the basis of 16S rRNA sequences. Int. J. Syst. Bacteriol. 43: 8–19Google Scholar
  27. Klug G (1993) Regulation of expression of photosynthesis genes in anoxygenic photosynthetic bacteria. Arch. Microbiol. 159: 397–404Google Scholar
  28. Körner H (1993) Anaerobic expression of nitric oxide reductase from denitrifyingPseudomonas stutzeri. Arch. Microbiol. 159: 410–416Google Scholar
  29. Körner H & Zumft WG (1989) Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture ofPseudomonas stutzeri. Appl. Env. Microbiol. 55: 1670–1676Google Scholar
  30. Lee JK & Kaplan S (1992)cis-acting regulatory elements involved in oxygen and light control ofpuc operon transcription inRhodobacter sphaeroides. J. Bacteriol. 174: 1146–1157Google Scholar
  31. Lodge J, Williams R, Bell A, Chan B & Busby S (1990) Comparison of promoter activities inEscherichia coli andPseudomonas aeruginosa: use of a new broad-host-range promoter-probe plasmid. FEMS Microbiol. Lett. 67: 221–226Google Scholar
  32. MacInnes JI, Kim JE, Lian C-J & Soltes GA (1990)Actinobacillus pleuropneumoniae hlyX gene homology with thefnr gene ofEscherichia coli. J. Bacteriol. 172: 4587–4592Google Scholar
  33. Meville S & Gunsalus RP (1990) Mutations infnr that alter anaerobic regulation of electron transport-associated genes inEscherichia coli. J. Biol. Chem. 265: 18733–18736Google Scholar
  34. Müller M & Hildebrandt A (1993) Nucleotide sequences of the 23S rRNA genes fromBordetella pertussis, B. parapertussis, B. bronchiseptica andB. avium, and their implications for phylogenetic analysis. Nucleic Acids Res. 21:3320.Google Scholar
  35. Müller-Breitkreutz K & Winkler UK (1993) Anaerobic expression of theVibrio fischeri lux regulon inE. coli is FNR-dependent. 7th International Symposium on Bioluminescence and Chemiluminescence. John Wiley & Sons, in press.Google Scholar
  36. Myers CR & Nealson KH (1990) Respiration-linked proton translocation coupled to anaerobic reduction of manganese (IV) and iron (III) inShewanella putrefaciens MR-1. J. Bacteriol. 172: 6232–6238Google Scholar
  37. Nealson KH (1977) Low oxygen is optimal for luciferase synthesis in some bacteria. Arch. Microbiol. 112: 9–16.Google Scholar
  38. Neidle EL & Kaplan S (1993) Expression of theRhodobacter sphaeroides hemA andhemT genes, encoding two 5-aminolevulinic acid synthase isoenzymes. J. Bacteriol. 175: 2292–2303Google Scholar
  39. Nishiyama M, Suzuki J, Kukimoto M, Ohnuki T, Horinouchi S & Beppu T (1993) Cloning and characterization of a nitrite reductase gene fromAlcaligenes faecalis and its expression inEscherichia coli. J. Gen. Microbiol. 139: 725–733Google Scholar
  40. Römermann D, Warrelmann J, Bender RA & Friedrich B (1989) AnrpoN-like gene ofAlcaligenes eutrophus andPseudomonas faecalis controls expression of diverse metabolic pathways, including hydrogen oxidation. J. Bacteriol. 171: 1093–1099Google Scholar
  41. Saffarini DA & Nealson KH (1993) Sequence and genetic characterization ofetrA, anfnr analog that regulates anaerobic respiration inShewanella putrefaciens MR-1. J. Bacteriol. 175: 7938–7944Google Scholar
  42. Sawers RG (1991) Identification and molecular characterization of a transcriptional regulator fromPseudomonas aeruginosa PAO1 exhibiting structural and functional similarity to the FNR protein ofEscherichia coli. Mol. Microbiol. 5: 1469–1481Google Scholar
  43. Schlüter A, Patschkowski T, Unden G & Priefer UB (1992) TheRhizobium leguminosarum FnrN protein is functionally similar toEscherichia coli Fnr and promotes heterologous oxygen-dependent activation of transcription. Mol. Microbiol. 6: 3395–3404Google Scholar
  44. Sharrocks AD, Green J & Guest JR (1990) In vivo and in vitro mutants of FNR the anaerobic transcriptional regulator ofE. coli. FEBS Lett. 270: 119–122Google Scholar
  45. Smith GB & Tiedje JM (1992) Isolation and characterization of a nitrite reductase gene and its use as a probe for denitrifying bacteria. Appl. Env. Microbiol. 58: 376–384Google Scholar
  46. Soltes GA & MacInnes JI (1994) Regulation of gene expression by the HlyX protein ofActinobacillus pleuropneumoniae. Microbiology In pressGoogle Scholar
  47. Spiro S (1992) An FNR-dependent promoter fromEscherichia coli is active and anaerobically inducible inParacoccus denitrificans. FEMS Microbiol. Lett. 98: 145–148Google Scholar
  48. Spiro S & Guest JR (1988) Inactivation of the FNR protein ofEscherichia coli by targeted mutagenesis in theN-terminal region. Mol. Microbiol. 2: 701–707Google Scholar
  49. Spiro S & Guest JR (1991) Adaptive responses to oxygen limitation inEscherichia coli. TIBS 16: 310–314Google Scholar
  50. Spiro S, Roberts RE & Guest JR (1989) FNR-dependent repression of thendh gene ofEscherichia coli and metal ion requirement for FNR-regulated gene expression. Mol. Microbiol. 3: 601–608Google Scholar
  51. Spiro S, Gaston KL, Bell AI, Roberts RE, Busby SJW & Guest JR (1990) Interconversion of the DNA-binding specificities of two related transcription regulators, CRP and FNR. Mol. Microbiol. 4: 1831–1838Google Scholar
  52. Steinrücke P & Ludwig B (1993) Genetics ofParacoccus denitrificans. FEMS Microbiol. Rev. 104:83–118.Google Scholar
  53. Trageser M & Unden G (1989) Role of cysteine residues and of metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration inEscherichia coli. Mol. Microbiol. 3: 593–599Google Scholar
  54. Upadhyaya NM, Scott KF, Tucker WT, Watson JM & Dart PJ (1992) Isolation and characterisation ofRhizobium (IC3342) genes that determine leaf curl induction in pigeon pea. Mol Plant Microb. Interact. 5: 129–143Google Scholar
  55. Viebrock A & Zumft WG (1988) Molecular cloning, heterologous expression, and primary structure of the structural gene for the copper enzyme nitrous oxide reductase from denitrifyingPseudomonas stutzeri. J. Bacteriol. 170: 4658–4668Google Scholar
  56. Waelkens F, Foglia A, Morel J-B, Fourment J, Batut J & Boistard P (1992) Molecular genetic analysis of theRhizobium meliloti fixK promoter: identification of sequences involved in positive and negative regulation. Mol. Microbiol. 6: 1447–1456Google Scholar
  57. Williams R, Bell A, Sims G & Busby S (1991) The role of two surface exposed loops in transcription activation by theEscherichia coli CRP and FNR proteins. Nucleic Acids Res. 19: 6705–6712Google Scholar
  58. Ye RW, Fries MR, Bezborodnikov SG, Averill BA & Tiedje JM (1993) Characterization of the structural gene encoding a copper-containing nitrite reductase and homology of this gene to other denitrifiers. Appl. Env. Microbiol. 59, 250–254Google Scholar
  59. Zimmermann A, Reimmann C, Galimand M & Haas D (1991) Anaerobic growth and cyanide synthesis ofPseudomonas aeruginosa depend onanr, a regulatory gene homologous withfnr ofEscherichia coli. Mol. Microbiol. 5: 1483–1490Google Scholar
  60. Zumft WG, Dreusch A, Löchelt S, Cuypers H, Friedrich B & Schneider B (1992) Derived amino acid sequences of thenosZ gene (respiratory N2O reductase) fromAlcaligenes eutrophus, Pseudomonas aeruginosa andPseudomonas stutzeri. Eur. J. Biochem. 208: 31–40Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Stephen Spiro
    • 1
  1. 1.School of Biological SciencesUniversity of East AngliaNorwichUK

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