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The FNR Modulon and FNR-Regulated Gene Expression

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Regulation of Gene Expression in Escherichia coli

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Abstract

In recent years it has been realized that the elaborate network of interacting metabolic processes operating in living bacteria is not maintained simply by controlling enzyme activities in response to specific metabolites (substrates, end-products and allosteric effectors) or by controlling enzyme synthesis via specific regulatory proteins that activate or repress relevant transcriptional units (genes, operons or regulons) in response to the corresponding metabolites (coeffectors). There is yet another tier of complexity imposed by global regulators which control families of transcriptional units in response to general metabolic or environmental factors. These families have been called regulatory networks or modulons. By belonging to one or more such modulons, the pattern of gene expression can be adapted to that required for a specific metabolic mode or physiological state. A major current challenge is to understand how multiple regulatory factors exert their various effects on a single transcriptional unit, and whether such interactions are sufficient to establish and maintain the complex coordinated metabolic networks operating under diverse physiological conditions, or whether other factors such as the regulation of regulatory gene expression, make a significant contribution to the overall process.

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References

  1. Spiro S, Guest JR. FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev 1990; 75:399–428.

    Article  Google Scholar 

  2. Unden G, Becker S, Bongaerts J et al. Oxygen regulated gene expression in facultatively anaerobic bacteria. Antonie van Leeuwenhoek 1994; 66, 3–23.

    Article  Google Scholar 

  3. Gunsalus RP. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol 1992; 174: 7069–7074.

    Google Scholar 

  4. Lin ECC, Iuchi S. Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria. Annu Rev Genet 1991; 25:361–387.

    Article  Google Scholar 

  5. Iuchi S, Lin ECC. Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol 1993; 9:9–15.

    Article  Google Scholar 

  6. Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev 1988; 52:190–232.

    Google Scholar 

  7. Stewart V. Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. Mol Microbiol 1993; 9:425–434.

    Article  Google Scholar 

  8. Lin ECC, Kuritzkes DR. Pathways for anaerobic electron transport. In: Neidhardt FC, ed. Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology. Washington: Amer Soc Microbiol, 1987:201–221.

    Google Scholar 

  9. Kaiser M, Sawers G. Pyruvate formate-lyase is not essential for nitrate respiration by Escherichia coli. FEMS Microbiol Lett 1994; 117:163–168.

    Article  Google Scholar 

  10. Clark DP. The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 1989;63:223–234.

    Article  Google Scholar 

  11. Rossmann R, Sawers G, Bock A. Mechanism of regulation of the formate-hydrogen-lyase pathway by oxygen, nitrate and pH: definition of the formate regulon. Mol Microbiol 1991; 5:2807–2814.

    Article  Google Scholar 

  12. Sauter M, Bohm R, Bock A. Mutational analysis of the Operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 1992; 6:1523–1532.

    Article  Google Scholar 

  13. Knappe J, Sawers G. A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate-formate-lyase system of Escherichia coli. FEMS Microbiol Rev 1990; 75:383–398.

    Article  Google Scholar 

  14. Quail MA, Haydon DJ, Guest JR. The pdhR-aceEF-lpd operon of Escherichia coli expresses the pyruvate dehydrogenase complex. Mol Microbiol 1994; 12:95–104.

    Article  Google Scholar 

  15. Engel P, Krämer R, Unden G. Transport of C4-dicarboxylates by anaerobically-grown Escherichia coli: energetics and mechanism of exchange, uptake and efflux. Eur J Biochem 1994; 174:605–614.

    Article  Google Scholar 

  16. Iuchi S, Aristarkhov A, Dong JM et al. Effects of nitrate respiration on expression of the arc-controlled operons encoding succinate dehydrogenase and flavin-linked L-lactate dehydrogenase. J Bacteriol 1994; 176:1695–1701.

    Google Scholar 

  17. Cotter PA, Gunsalus RP. Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli. FEMS Microbiol Lett 1992; 91:31–36.

    Article  Google Scholar 

  18. Hassan HM, Sun HCH. Regulatory roles of Fnr, Fur and Arc in expression of manganese-containing superoxide dismutase in Escherichia coli. Proc Natl Acad Sci USA 1992; 89:3217–3221.

    Article  Google Scholar 

  19. Fu HA, Iuchi S, Lin ECC. The requirement of arcA and fnr for peak expression of the cyd operon in Escherichia coli under microaerobic conditions. Mol Gen Genet 1991; 226:209–213.

    Article  Google Scholar 

  20. Sawers G. Specific transcriptional requirements for positive regulation of the anaerobically inducible pfl operon by ArcA and FNR. Mol Microbiol 1993; 10:737–747.

    Article  Google Scholar 

  21. McCleary R, Stock JB, Ninfa AJ. Is acetyl phosphate a global signal in Escherichia col?. J Bacteriol 1993; 175: 2793–2798.

    Google Scholar 

  22. Wanner BL, Wilmes-Riesenberg MR. Involvement of phosphotransacetylase, acetate kinase and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J Bacteriol 1993; 174: 2124–2130.

    Google Scholar 

  23. Rabin RS, Stewart V. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate-and nitrite-regulated gene expression in Escherichia coli-YA2. J Bacteriol 1993; 175:3259–3268.

    Google Scholar 

  24. Lutz S, Jacobi A, Schlensog V et al. Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol Microbiol 1991; 5:123–135.

    Article  Google Scholar 

  25. Riley M. Functions of the gene products of Escherichia coli. Microbiol Rev 1993; 57:862–952.

    Google Scholar 

  26. Green J, Trageser JM, Six S et al. Characterization of the FNR protein of Escherichia coli, an iron-binding transcriptional regulator. Proc Roy Soc Lond B 1991; 244:137–144.

    Article  Google Scholar 

  27. Sharrocks AD, Green J, Guest JR. FNR activates and represses transcription in vitro. Proc Roy Soc Lond B 1991; 245:219–226.

    Article  Google Scholar 

  28. Green J, Guest JR. Regulation of transcription at the ndh promoter of Escherichia coli by FNR and novel factors. Mol Microbiol 1994; 12:433–444.

    Article  Google Scholar 

  29. Takahashi K, Hattori T, Nakanishi T et al. Repression of in vitro transcription of the Escherichia coli far and narX genes by FNR protein. FEBS Lett 1994; 340: 59–64.

    Article  Google Scholar 

  30. Suppmann B, Sawers G. Isolation and characterization of hypophosphite-resistant mutants of Escherichia coli: identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter. Mol Microbiol 1994; 11:965–982.

    Article  Google Scholar 

  31. Chen Y-M, Lin ECC. Regulation of the adhE gene, which encodes ethanol dehydrogenase in Escherichia coli. J Bacteriol 1991; 173:8009–8013.

    Google Scholar 

  32. Compan I, Touati D. Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA. Mol Microbiol 1994; 11:955–964.

    Article  Google Scholar 

  33. Schultz SC, Shields GC, Steitz TA. Crystal structure of a CAP-DNA complex: the DNA is bent by 90. Science 1991; 253:1001–1007.

    Article  Google Scholar 

  34. Spiro S, Gaston KL, Bell AI et al. Interconversion of the DNA-binding specificities of two related transcription regulators, CRP and FNR. Mol Microbiol 1990; 4:1831–1838.

    Article  Google Scholar 

  35. Green J, Sharrocks AD, Green B et al. Properties of FNR proteins substituted at each of the five cysteine residues. Mol Microbiol. 1993; 8:61–68.

    Article  Google Scholar 

  36. Unden G, Duchene A. On the role of cyclic AMP and the FNR protein in E. coli growing anaerobically. Arch Microbiol 1987; 147:195–200.

    Article  Google Scholar 

  37. Bell A, Busby S. Location and orientation of an activating region in the Escherichia coli transcription factor, FNR. Mol Microbiol 1994; 11:383–390.

    Article  Google Scholar 

  38. Williams R, Bell A, Sims G et al. The role of two surface exposed loops in transcription activation by the Escherichia coli CRP and FNR proteins. Nucl Acids Res 1991; 19:6705–6712.

    Article  Google Scholar 

  39. Sharrocks AD, Green J, Guest JR. In vivo and in vitro mutants of FNR, the anaerobic transcriptional regulator of E. coli. FEBS Lett 1990; 270:119–132.

    Article  Google Scholar 

  40. Melville SB, Gunsalus RP. Mutations in fnr that alter anaerobic regulation of electron transport-associated genes in Escherichia coli. J Biol Chem 1990; 265:18733–18736.

    Google Scholar 

  41. Green J, Guest JR. Activation of FNR-dependent transcription by iron: an in vitro switch for FNR. FEMS Microbiol Lett 1993; 113:219–222.

    Article  Google Scholar 

  42. Lazazzera BA, Bates DM, Kiley PJ. The activity of the Escherichia coli transcription factor FNR is regulated by a change in oligomeric state. Genes Dev 1993; 7:1993–2005.

    Article  Google Scholar 

  43. Bell A, Cole JA, Busby SJW. Molecular genetic analysis of an FNR-dependent anaerobically inducible Escherichia coli promoter. Mol Microbiol 1990; 4:1753–1763.

    Article  Google Scholar 

  44. Green J, Guest JR. A role for iron in transcriptional activation by FNR. FEBS Lett 1993; 329:55–58.

    Article  Google Scholar 

  45. Adhya S, Gottesman M, Garges S. Promoter resurrection by activators — a minireview. Gene 1993; 132:1–6.

    Article  Google Scholar 

  46. Kolb A, Busby S, Buc H et al. Transcriptional regulation by cAMP and its receptor protein. Ann Rev Biochem 1993; 62:747–795.

    Article  Google Scholar 

  47. Collado-Vides J, Magasanik B, Gralla JD. Control site location and transcriptional regulation in Escherichia coli. Microbiol Rev 1991; 55:371–394.

    Google Scholar 

  48. 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; 174:4935–4942.

    Google Scholar 

  49. Stewart V. Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol 1982; 151:1320–1325.

    Google Scholar 

  50. Tyson KL, Bell AI, Cole JA et al. Definitioin of nitrite and nitrate response elements at the anaerobically inducible Escherichia coli nirB promoter—interactions between FNR and NarL. Mol Microbiol 1993; 7:151–157.

    Article  Google Scholar 

  51. Kiley PJ, Reznikoff W. Fnr mutants that activate gene expression in the presence of oxygen. J Bacteriol 1991; 173:16–22.

    Google Scholar 

  52. Walker MS, Demoss JA. Role of alternative promoter elements in transcription from the nar promoter of Escherichia coli. J Bacteriol 1992; 174:1119–1123.

    Google Scholar 

  53. Schröder I, Darie S, Gunsalus RP. Activation of the Escherichia coli nitrate reductase (narGHJI) operon by NarL and Fnr requires integration host factor. J Biol Chem 1992; 268:771–774.

    Google Scholar 

  54. Unden G, Trageser M, Duchene A. Effect of positive redox potentials (>+400mV) on the expression of anaerobic respiratory enzymes of Escherichia coli. Mol Microbiol 1990; 4:315–319.

    Article  Google Scholar 

  55. Bogachev AV, Murtazina RA, Skulacher VP. Cytochrome d induction in Escherichia coli growing under unfavourable conditions. FEBS Lett 1993; 336:75–78.

    Article  Google Scholar 

  56. Eraso JM, Weinstock GM. Anaerobic control of colicin El production. J Bacteriol 1992; 174:5101–5109.

    Google Scholar 

  57. Jennings MP, Beacham IR. Co-dependent positive regulation of the ansB promoter of Escherichia coli by CRP and the FNR protein: a molecular analysis. Mol Microbiol 1993; 9:155–164.

    Article  Google Scholar 

  58. Zhang X, Ebright RH. Substitution of 2 base pairs (1 base pair per DNA half-site) within the Escherichia coli lac promoter DNA site for catabolic gene activator protein places the lac promoter in the FNR regulon. J Biol Chem 1990; 265:12400–12403.

    Google Scholar 

  59. West D, Williams R, Rhodius V et al. Interactions between the Escherichia coli cyclic AMP receptor protein and RNA polymerase at Class II promoters. Mol Microbiol 1993; 10: 789–797.

    Article  Google Scholar 

  60. Kumar A, Grimes B, Fujita N et al. Role of sigma 70 subunit of Escherichia coli RNA polymerase in transcription activation. J Mol Biol 1994; 235:405–413.

    Article  Google Scholar 

  61. Lombardo MJ, Bagga D, Miller CG. Mutations in rpoA affect expression of anaerobically regulated genes in Salmonella typhimurium. J Bacteriol 1991; 173:7511–7518.

    Google Scholar 

  62. Fischer HM, Bruderer T, Hennecke H. Essential and non-essential domains in the Bradyrhizobium japonicum NifA protein: identification of indispensible cysteine residues potentially involved in redox activity and/or metal binding. Nucl Acids Res 1988; 16:2207–2224.

    Article  Google Scholar 

  63. Spiro S, Roberts R, Guest JR. FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR regulated gene expression. Mol Microbiol 1989; 3:601–608.

    Article  Google Scholar 

  64. Trageser M, Unden G. Role of cysteine residues and of metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration in Escherichia coli. Mol Microbiol 1989; 3:593–599.

    Article  Google Scholar 

  65. Engel P, Trageser M, Unden G. Reversible interconversion of the functional state of the gene regulator FNR from Escherichia coli in vivo by O2 and iron availability. Arch Microbiol 1991; 156:463–470.

    Google Scholar 

  66. Niehaus F, Hantke K, Unden G. Iron content and FNR-dependent gene regulation in Escherichia coli. FEMS Microbiol Lett 1991; 84:319–324.

    Article  Google Scholar 

  67. Sawers RG, Zehelein E, Bock A. Two-dimensional gel electrophoretic analysis of Escherichia coli proteins: influence of various anaerobic growth conditions and the fnr gene product on cellular protein composition. Arch Microbiol 1988; 149: 240–244.

    Article  Google Scholar 

  68. Pascal M-C, Bonnefoy V, Fons M et al. Use of gene fusions to study the expression of fnr, the regulatory gene of anaerobic electron transfer in Escherichia coli. FEMS Microbiol Lett 1986; 36:35–40.

    Article  Google Scholar 

  69. Sokes GA, Maclnnes JI. Regulation of gene expression by the HlyX protein of Actinobacillus pleuropneumoniae. Microbiol 1994; 140: 839–845.

    Article  Google Scholar 

  70. Spencer M, Guest JR. Isolation and properties of fumarate reductase mutants of Escherichia coli. J Bacteriol 1973; 114: 563–570.

    Google Scholar 

  71. Amarasingham CR, Davis BD. Regulation of -ketoglutarate dehydrogenase formation in Escherichia coli. J Biol Chem 1965; 240: 3664–3668.

    Google Scholar 

  72. Kucera I, Matchova I, Spiro S. Respiratory inhibitors activate an FNR-like regulatory protein in Parracoccus denitrificans. Biochem Mol Biol Int 1994; 32:245–250.

    Google Scholar 

  73. Giordano G, Grillet L, Rosset R et al. Characterization of an Escherichia coli mutant that is sensitive to chlorate when grown aerobically. Biochem J 1978; 176: 553–561.

    Google Scholar 

  74. Irvine AS, Guest JR. Lactobacillus casei contains a member of the CRP-FNR family. Nucl Acids Res 1993; 21:753.

    Article  Google Scholar 

  75. Spiro S. The FNR family of transcriptional regulators. Antonie van Leeuwenhoek 1994; 66, 23–36.

    Article  Google Scholar 

  76. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.5c, 1993. University of Washington, Seattle.

    Google Scholar 

  77. Lampdis R, Gross R, Sokolovic Z et al. The virulence regulator of Listeria ivanovii is highly homologous to PfrA from Listeria monocytogenes and both belong to the Crp-Fnr family of transcription regulators. Mol Microbiol 1994; 13:141–151.

    Article  Google Scholar 

  78. Van Spanning RJ, Anthonius M, De Boer PN et al. Nitrite and nitric oxide reduction in Paracoccus denitrificans is under the control of NNR, a regulatory protein that belongs to the FNR family of transcriptional activators. FEBS Lett 1995; in press.

    Google Scholar 

  79. Ziegelhoffer EC, Kiley PJ. In vitro analysis of a constitutively active mutant form of the Escherichia coli global transcription factor FNR. J Mol Biol 1995; 245: 351–361.

    Article  Google Scholar 

  80. Khoroshilova N, Beinert H, Kiley PJ. Association of a polynuclear iron-sulfur center with a mutant FNR protein enhances DNA-binding. Proc Natl Acad Sci USA 1995; 92: 2499–2505.

    Article  Google Scholar 

  81. Hidalgo E, Demple B. An iron-sulphur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J 1994; 13: 138–146.

    Google Scholar 

  82. Kullick I, Toledano MB, Tartaglia LA et al. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 1995; 177: 1275–1284.

    Google Scholar 

  83. Gilles-Gonzalez MA, Ditta GS, Helinski DR. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 1991; 350: 170–172.

    Article  Google Scholar 

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  1. John R. Guest
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  2. Jeffrey Green
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  3. Alistair S. Irvine
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  4. Stephen Spiro
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© 1996 R.G. Landes Company

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Guest, J.R., Green, J., Irvine, A.S., Spiro, S. (1996). The FNR Modulon and FNR-Regulated Gene Expression. In: Regulation of Gene Expression in Escherichia coli . Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-8601-8_16

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  • DOI: https://doi.org/10.1007/978-1-4684-8601-8_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-8603-2

  • Online ISBN: 978-1-4684-8601-8

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