Antonie van Leeuwenhoek

, Volume 66, Issue 1–3, pp 3–22 | Cite as

Oxygen regulated gene expression in facultatively anaerobic bacteria

  • G. Unden
  • S. Becker
  • J. Bongaerts
  • J. Schirawski
  • S. Six
Research Articles


In facultatively anaerobic bacteria such asEscherichia coli, oxygen and other electron acceptors fundamentally influence catabolic and anabolic pathways.E. coli is able to grow aerobically by respiration and in the absence of O2 by anaerobic respiration with nitrate, nitrite, fumarate, dimethylsulfoxide and trimethylamine N-oxide as acceptors or by fermentation. The expression of the various catabolic pathways occurs according to a hierarchy with 3 or 4 levels. Aerobic respiration at the highest level is followed by nitrate respiration (level 2), anaerobic respiration with the other acceptors (level 3) and fermentation. In other bacteria, different regulatory cascades with other underlying principles can be observed. Regulation of anabolism in response to O2 availability is important, too. It is caused by different requirements of cofactors or coenzymes in aerobic and anaerobic metabolism and by the requirement for different O2-independent biosynthetic routes under anoxia. The regulation mainly occurs at the transcriptional level. InE. coli, 4 global regulatory systems are known to be essential for the aerobic/anaerobic switch and the described hierarchy. A two-component sensor/regulator system comprising ArcB (sensor) and ArcA (transcriptional regulator) is responsible for regulation of aerobic metabolism. The FNR protein is a transcriptional sensor-regulator protein which regulates anaerobic respiratory genes in response to O2 availability. The gene activator FhlA regulates fermentative formate and hydrogen metabolism with formate as the inductor. ArcA/B and FNR directly respond to O2, FhlA indirectly by decreased levels of formate in the presence of O2. Regulation of nitrate/nitrite catabolism is effected by two 2-component sensor/regulator systems NarX(Q)/NarL(P) in response to nitrate/nitrite. Co-operation of the different regulatory systems at the target promoters which are in part under dual (or manifold) transcriptional control causes the expression according to the hierarchy. The sensing of the environmental signals by the sensor proteins or domains is not well understood so far. FNR, which acts presumably as a cytoplasmic ‘one component’ sensor-regulator, is suggested to sense directly cytoplasmic O2-levels corresponding to the environmental O2-levels.

Key words

facultatively anaerobic bacteria anaerobic gene regulation oxygen aerobic/anaerobic respiration metabolism 


ArcA or B

aerobic respiration control protein A or B




fumarate and nitrate reduction (or regulation)


trimethylamine N-oxide


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  1. Alexander K & Young IG (1978) Alternative hydroxylases for the aerobic and anaerobic biosynthesis of ubiquinone inEscherichia coli. Biochemistry 17: 4750–4755Google Scholar
  2. Andersson DI (1992) Involvement of the ArcA system in redox regulation of thecob operon inSalmonella typhimurium. Mol. Microbiol. 6: 1491–1494Google Scholar
  3. Andrews SC, Shipley D, Keen JN, Findlay JBC, Harrison PM & Guest JR (1992) The haemoglobin-like protein (HMP) ofEscherichia coli has ferrisiderophore reductase activity and its C-terminal domain shares homology with ferredoxin NADP+ reductases. FEBS Lett. 302: 247–252Google Scholar
  4. 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
  5. Barman TE (1974) Enzyme handbook, Supplement I; Springer, BerlinGoogle Scholar
  6. Belaich A & Belaich JP (1976) Microcalorimetric study of the anaerobic growth ofEscherichia coli: growth thermograms in a synthetic medium. J. Bacteriol. 125: 14–18Google Scholar
  7. Bell AI, Gaston KL, Cole JA & Busby SJW (1989) Cloning of binding sequences for theEscherichia coli transcription activators, FNR and CRP: location of bases involved in discrimination between FNR and CRP. Nucl. Acids Res. 17: 3865–3874Google Scholar
  8. Bentley R & Meganathan R (1987) Biosynthesis of the isoprenoid quinones ubiquinone and menaquinone in ‘Escherichia coli andSalmonella typhimurium’. In: Neidhardt FC (Ed) American Society for Microbiology, WashingtonGoogle Scholar
  9. Bianchi V, Reichard P. Eliasson R, Pontis E, Krook M, Jörnvall H & Haggard-Ljungquist E (1993)Escherichia coli ferredoxin NADP+ reductase: activation ofE. coli anaerobic ribonucleotide reduction, cloning of the gene (fpr), and overexpression of the protein. J. Bacteriol. 175: 1590–1595Google Scholar
  10. Birkmann A, Sawers RG & Böck A (1987) Involvement of thentrA gene product in the anaerobic metabolism ofEscherichia coli. Mol. Gen. Genet. 210: 535–542Google Scholar
  11. Bott M, Bollinger M & Hennecke H (1990) Genetic analysis of the cytochrome c-aa3 branch of theBradyrhizobium japonicum respiratory chain. Mol. Microbiol. 4: 2147–2157Google Scholar
  12. Busby S (1992) Kinked, curved or bent but certainly not going straight. Curr. Biol. 2: 53–55Google Scholar
  13. Calhoun MW, Oden KL, Gennis RB, Teixeira de Mattos MJ & Neijssel OM (1993) Energetic efficiency ofEscherichia coli: effects of mutations in components of the aerobic respiratory chain. J. Bacteriol. 175: 3020–3025Google Scholar
  14. Chiang RC, Cavicchioli R & Gunsalus RP (1992) Identification and characterization ofnarQ, a second nitrate sensor-transmitter for nitrate-dependent gene regulation inEscherichia coli. Mol. Microbiol. 6: 1913–1923Google Scholar
  15. Chippaux M, Giudici D, Aboujaoude A, Casse F & Pascal M (1978) A mutation leading to the total lack of nitrite reductase activity inEscherichia coli K-12. Mol. Gen. Genet. 182: 477–479Google Scholar
  16. Cotter PA & Gunsalus RP (1992) Contribution of thefnr andarcA gene products in coordinate regulation of cytochromeo andd oxidase (cyoABCD andcydAB) genes inEscherichia coli. FEMS Microbiol. Lett. 91: 31–36Google Scholar
  17. Cuypers H & Zumft WG (1993) Anaerobic control of denitrification inPseudomonas stutzeri escapes mutagenesis of anfnr-like gene. J. Bacteriol. 175: 7236–7246Google Scholar
  18. Daniel RM, Limmer AW, Steele KW & Smith IM (1982) Anaerobic growth, nitrate reduction and denitrification in 46Rhizobium strains. J. Gen. Microbiol. 128: 1811–1815Google Scholar
  19. Demple B & Amábile-Cuevas CF (1991) Redox redux: the control of oxidative stress responses. Cell 67: 837–839Google Scholar
  20. Dispensa M, Thomas CT, Kim MK, Perrotta JA, Gibson J & Harwood CS (1992) Anaerobic growth ofRhodopseudomonas palustris on 4-hydroxybenzoate is dependent AadR, a member of the cyclic AMP receptor protein family of transcriptional regulators. J. Bacteriol. 174: 5803–5813Google Scholar
  21. Eiglmeier K, Honoré N, Iuchi S, Lin ECC & Cole ST (1989) Molecular genetic analysis of FNR-dependent promoters. Mol. Microbiol. 3: 869–878Google Scholar
  22. Engel P, Trageser M & Unden G (1991) Reversible interconversion of the functional state of the gene regulator FNR fromEscherichia coli in vivo by O2 and iron availability. Arch. Microbiol. 156: 463–470Google Scholar
  23. Engel P, Krämer R & Unden G (1992) Anaerobic fumarate transport inEscherichia coli by afnr-dependent dicarboxylate uptake system which is different from aerobic dicarboxylate uptake. J. Bacteriol. 174: 5533–5539Google Scholar
  24. Engel P, Krämer R & Unden G (1994) Transport of C4-dicarboxylates by anaerobically grownEscherichia coli: Energetics and mechanisms of exchange, uptake and efflux. Eur. J. Biochem. In pressGoogle Scholar
  25. Fontecave M, Eliasson R & Reichard P (1989) Oxygen-sensitive ribonucleoside triphosphate reductase is present in anaerobicEscherichia coli. Proc. Natl. Acad. Sci. USA 86: 2147–2151Google Scholar
  26. Fu H-A, Iuchi S & Lin ECC (1991) The requirement of ArcA and Fnr for peak expression of thecyd operon inEscherichia coli under microaerophilic conditions. Mol. Gen. Genet. 226: 209–213Google Scholar
  27. Gal A, Schuster G, Frid D, Canaani O, Schwieger H-G & Ohad I (1988) Role of the cytochrome b6 f complex in the redox-controlled activity ofAcetabularia thylakoid protein kinase. J. Biol. Chem. 263: 7785–7791Google Scholar
  28. Gibson LCD, McGlynn P, Chaudhri M & Hunter CN (1992) A putative anaerobic coproporphyrinogen III oxidase inRhodobacter sphaeroides II. Analysis of a region of the genome encodinghemF and thepuc operon. Mol. Microbiol. 6: 3171–3186Google Scholar
  29. Gilles-Gonzalez MA, Ditta GS & Helinski DR (1991) A hemoprotein with kinase activity encoded by the oxygen sensor ofRhizobium meliloti. Nature 350: 170–172Google Scholar
  30. Green J & Guest JR (1993) A role for iron in transcriptional activation by FNR. FEBS Lett. 329: 55–58Google Scholar
  31. 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. B 244: 137–144Google Scholar
  32. 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
  33. Grieshaber MK, Hardewig I, Kreutzer U, Schneider A & Völkel S (1992) Hypoxia and sulfide tolerance in some marine invertebrates. Verh. Dtsch. Zool. Ges. 85: 55–76Google Scholar
  34. Gross R, Arico B & Rappuoli R (1989) Families of bacterial signal-transducing proteins. Mol. Microbiol. 3: 1661–1667Google Scholar
  35. Gunsalus RP (1992) Control of electron flow inEscherichia coli: Coordinated transcription of respiratory pathway genes. J. Bacteriol. 174: 7069–7074Google Scholar
  36. Gunsalus RP, Kalman LV & Stewart RR (1989) Nucleotide sequence of thenarL gene that is involved in global regulation of nitrate controlled respiratory genes ofEscherichia coli. Nucleic Acids Res. 17: 1965–1975Google Scholar
  37. Harborne NR, Griffiths L, Busby SJW & Cole JA (1992) Transcriptional control, translation and function of the products of the five open reading frames of theEscherichia coli nir operon. Mol. Microbiol. 6: 2805–2813Google Scholar
  38. Harder J & Follmann H (1990) Identification of a free radical and oxygen dependence of ribonucleotide reductase in yeast. Free Rad. Res. Comms. 10: 281–286Google Scholar
  39. Hartmann R, Sickinger H & Oesterhelt D (1980) Anaerobic growth of Halobacteria. Proc. Natl. Acad. Sci USA 77: 3821–3825Google Scholar
  40. Helmann JD, Ballard BT & Walsh CT (1990) The MerR metalloregulatory protein binds mercuric ion as a tricoordinate metal-bridged dimer. Science 247: 946–948Google Scholar
  41. Holmgren A (1980) Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264: 13963–13966Google Scholar
  42. Imlay JA & Fridovich I (1991) Assay of metabolic superoxide production inEscherichia coli. J. Biol. Chem. 266: 6957–6965Google Scholar
  43. Ingledew WJ & Poole RK (1984) The respiratory chains ofEscherichia coli. Microbiol. Rev. 48: 222–271Google Scholar
  44. Irvine AS & Guest JR (1993)Lactobacillus casei contains a member of the CRP-FNR family. Nucleic Acids Res. 21: 753Google Scholar
  45. Ishihama A (1993) Protein-protein communication within the transcription apparatus. J. Bacteriol. 175: 2483–2489Google Scholar
  46. Iuchi S & Lin ECC (1988)arcA (dye), a global regulatory gene inEscherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. USA 85: 1888–1892Google Scholar
  47. Iuchi S, Cameron DC & Lin ECC (1989) A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathway ofEscherichia coli. J. Bact. 171: 868–873Google Scholar
  48. Iuchi S, Matsuda Z, Fujiwara T & Lin ECC (1990b) ThearcB gene ofEscherichia coli encodes a sensor-regulator protein for anaerobic repression of thearc modulon. Mol. Microbiol. 4: 715–727Google Scholar
  49. Iuchi S & Lin ECC (1992) Purification and phosphorylation of the Arc regulatory components ofEscherichia coli. J. Bacteriol. 174: 5617–5623Google Scholar
  50. Iuchi S & Lin ECC (1993) Adaptation ofEscherichia coli to redox environments by gene expression. Molec. Microbiol. 9: 9–15Google Scholar
  51. Jayaraman P-S, Cole JA & Busby SJW (1989) Mutational analysis of the nucleotide sequences at the FNR-dependentnirB promoter inEscherichia coli. Nucl. Acids Res. 17: 135–145Google Scholar
  52. Jayaraman P-S, Gaston KL, Cole JA & Busby SJW (1988) ThenirB promoter ofEscherichia coli: Location of the nucleotide sequences essential for regulation by oxygen, the FNR protein and nitrite. Mol. Microbiol. 2: 527–530Google Scholar
  53. Jensen LH (1974) X-ray structural studies of ferredoxin and related electron carriers. Ann. Rev. Biochem. 43: 461–474Google Scholar
  54. Jeter RM, Olivera BM & Roth JR (1984)Salmonella typhimurium synthesizes cobalamin (vitamin B12)de novo under anaerobic growth conditions. J. Bacteriol. 159: 206–213Google Scholar
  55. Jones HM & Gunsalus RP (1987) Regulation ofEscherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and thefnr gene product. J. Bacteriol. 169: 3340–3349Google Scholar
  56. Kay WW & Kornberg HL (1971) Transport of C4-dicarboxylic acids byEscherichia coli. Eur. J. Biochem. 18: 274–281Google Scholar
  57. Kiley PJ & Kaplan S (1988) Molecular genetics of photosynthetic membrane biosynthesis inRhodobacter sphaeroides. Microbiol. Rev. 52: 50–69Google Scholar
  58. Kiley PJ & Reznikoff W (1991) Fnr mutants that activate gene expression in the presence of oxygen. J. Bacteriol. 173: 16–22Google Scholar
  59. Kletzin A (1992) Molecular characterization of thesor gene, which encodes the sulfur oxygenase/reductase of the thermoacidophilic archaeumDesulfurolobus ambivalens. J. Bacteriol. 174: 5854–5859Google Scholar
  60. Klug G (1993) Regulation of expression of photosynthetic genes in anoxygenic photosynthetic bacteria. Arch. Microbiol. 159: 397–404Google Scholar
  61. Knappe J & Sawers G (1990) A radical-chemical route to acetylCoA: the anaerobically induced pyruvate formate-lyase system ofEscherichia coli. FEMS Microbiol. Rev. 75: 383–398Google Scholar
  62. Lambden PR & Guest JR (1976) Mutants ofEscherichia coli unable to use fumarate as an anaerobic electron acceptor. J. Gen. Microbiol. 97: 145–160Google Scholar
  63. Lascelles J (1978) Regulation of pyrrole synthesis. In: Clayton RK & Sistrom WR (Eds) The photosynthetic bacteria (pp 795–808). Plenum Press, New YorkGoogle Scholar
  64. Leonardo MR, Cunningham PR & Clark DP (1993) Anaerobic regulation of theadhE gene, encoding the fermentative alcohol dehydrogenase ofEscherichia coli. J. Bacteriol. 175: 870–878Google Scholar
  65. Li SF & DeMoss JA (1988) Location of sequences in thenar promoter ofEscherichia coli required for the regulation by Fnr and NarL. J. Biol. Chem. 263: 13700–13705Google Scholar
  66. Li J & Stewart V (1992) Localization of upstream sequence elements required for nitrate and anaerobic induction offdn (formate dehydrogenase-N) operon expression inEscherichia coli K-12. J. Bacteriol. 174: 4935–4942Google Scholar
  67. Lin ECC & Iuchi S (1991) Regulation of gene expression in fermentative and respiratory systems inEscherichia coli and related bacteria. Annu. Rev. Genet. 25: 361–387Google Scholar
  68. Lombardo M-J, Bagga D & Miller CG (1991) Mutations inrpoA affect expression of anaerobically regulated genes inSalmonella typhimurium. J. Bacteriol. 173: 7511–7518Google Scholar
  69. Lorenzen JP, Kröger A & Unden G (1993) Regulation of anaerobic respiratory pathways inWolinella succinogenes by the presence of electron acceptors. Arch. Microbiol. 159: 477–483Google Scholar
  70. Lutz S, Böhm R, Beier A & Böck A (1990) Characterization of divergent NtrA-dependent promoters in the anaerobically expressed gene cluster coding for hydrogenase 3 components inEscherichia coli. Molec. Microbiol. 4: 13–20Google Scholar
  71. McInnes 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
  72. Melville SB & Gunsalus RP (1990) Mutations infnr that alter anaerobic regulation of electron transport-associated genes inEscherichia coli. J. Biol. Chem. 256: 18733–18736Google Scholar
  73. Miles JS & Guest JR (1987) Molecular genetic aspects of the citric acid cycle ofEscherichia coli. In: Kay J & Weitzman PDJ (Eds) Krebs' citric acid cycle. Biochem. Soc. Symposium No. 54 (pp 45–65). The Biochemical Society, LondonGoogle Scholar
  74. Misra HP (1974) Generation of superoxide free radical during the autoxidation of thiols. J. Biol. Chem. 7: 2151–2155Google Scholar
  75. Müller-Breitkreutz K, Abrahams M & Winkler U (1991) Regulation der Biolumineszenz vonVibrio fischeri durch Anaerobiose und das FNR-Protein. Abstr. 43. Annu. Meeting Dtsch. Ges. Hyg. Microbiol. 1991Google Scholar
  76. Murata K & Kimura A (1982) Some properties of glutathione biosynthesis-deficient mutants ofEscherichia coli B. J. Gen. Microbiol. 128: 1047–1052Google Scholar
  77. Neidle EL & Kaplan S (1993) Expression of theRhodobacter sphaeroides hemA andhemT genes, encoding two 5-aminolevulinic acid synthase isozymes. J. Bacteriol. 175: 2292–2303Google Scholar
  78. Newman BM & Cole JA (1978) The chromosomal location and pleiotropic effects of mutations of thenirA + gene ofEscherichia coli: The essential role ofnirA + in nitrite reduction and in other anaerobic redox reactions. J. Gen. Microbiol. 106: 1–12Google Scholar
  79. Niehaus F, Hantke K & Unden G (1991) Iron content and FNR-dependent gene regulation inEscherichia coli. FEMS Microbiol. Lett. 84: 319–324Google Scholar
  80. Noji S & Taniguchi S (1987) Molecular oxygen controls nitrate transport ofEscherichia coli nitrate respiring cells. J. Biol. Chem. 262: 9441–9443Google Scholar
  81. Nunoshiba T, Hidalgo E, Amábile-Cuevas CF & Demple B (1992) Two-stage control of an oxidative stress regulon: theEscherichia coli SoxR protein triggers redox-inducible expression of thesoxS regulatory gene. J. Bacteriol. 174: 6054–6060Google Scholar
  82. Oren A (1991) Anaerobic growth of halophilic archaeobacteria by reduction of fumarate. J. Gen. Microbiol. 137: 1387–1390Google Scholar
  83. Pörtner H-O, Kreutzer U, Siegmund B, Heisler N & Grieshaber MK (1984) Metabolic adaption of the intertidal wormSipunculus nudus to functional and environmental hypoxia. Marine Biology 79: 237–247Google Scholar
  84. Rabin RS & Stewart V (1992) Either of two functionally redundant sensor proteins, NarX or NarQ, is sufficient for nitrate regulation inEscherichia coli K-12. Proc. Natl. Acad. Sci. USA 89: 8419–8423Google Scholar
  85. Rabin RS, Collins LA & Stewart V (1992)In vivo requirement of integration host factor fornar (nitrate reductase) operon expression inEscherichia coli K-12. Proc. Natl. Acad. Sci. USA 89: 8701–8705Google Scholar
  86. Rabin RS & Stewart V (1993) Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression inEscherichia coli K-12. J. Bacteriol. 175: 3259–3268Google Scholar
  87. Rabinowitch HD, Sklan D, Chace DH, Stevens RD & Fridovich I (1993)Escherichia coli produces linoleic acid during late stationary phase. J. Bacteriol. 175: 5324–5328Google Scholar
  88. Rivers SL, McNairn E, Blasco F, Giordano G & Boxer DH (1993) Molecular genetic analysis of themoa operon ofEscherichia coli K-12 required for molybdenum cofactor biosynthesis. Mol. Microbiol. 8: 1071–1081Google Scholar
  89. Robertson LA & Kuenen JG (1984) Aerobic denitrification: a controversy revived. Arch. Microbiol. 139: 351–354Google Scholar
  90. Rödel W, Plaga W, Frank R & Knappe J (1988) Primary structures ofEscherichia coli pyruvate formate-lyase and pyruvate formatelyase-activating enzyme deduced from the DNA nucleotide sequences. Eur. J. Biochem. 177: 153–158Google Scholar
  91. Rossmann R, Sawers G & Böck A (1991) Mechanism of regulation of the formate-hydrogen-lyase pathway by oxygen, nitrate and pH: definition of the formate regulon. Molec. Microbiol. 5: 2807–2814Google Scholar
  92. Sauter M, Böhm R & Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation inEscherichia coli. Molec. Microbiol. 6: 1523–1532Google Scholar
  93. Sawers RG (1991) Identification and molecular characterization of a transcriptional regulator fromPseudomonas aeruginosa PA01 exhibiting structural and functional similarity to the FNR protein ofEscherichia coli. Mol. Microbiol. 5: 1469–1481Google Scholar
  94. Sawers G (1993) Specific transcriptional requirements for positive regulation of the anaerobically induciblepfl operon by ArcA and FNR. Mol. Microbiol. 10: 737–748Google Scholar
  95. Sawers G & Suppmann (1992) Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J. Bacteriol. 174: 3474–3478Google Scholar
  96. Sawers G, Wagner AFV & Böck A (1989) Transcriptional initiation at multiple promoters of thepfl gene by σ70-dependent transcriptionin vitro and heterologous expression inPseudomonas putida in vivo. J. Bacteriol. 171: 4930–4937Google Scholar
  97. Schlensog V & Böck A (1990) Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system ofE. coli. Mol. Microbiol. 4: 1319–1327Google Scholar
  98. Schlüter A, Patschkowski T, Unden G & Priefer U (1992) TheRhizobium leguminosarum FNRN protein is functionally similar toEscherichia coli FNR and promotes heterologous oxygen-dependent activation of transcription. Molec. Microbiol. 6: 3395–3404Google Scholar
  99. Schröder I, Darie S & Gunsalus RP (1993) Activation of theEscherichia coli nitrate reductase (narGHJI) operon by NarL and FNR requires integration host factor. J. Biol. Chem. 268: 771–774Google Scholar
  100. Sharrocks AD, Green J & Guest JR (1990)In vivo andin vitro mutants of FNR, the anaerobic transcriptional regulator ofEscherichia coli. FEBS Lett. 270: 119–122Google Scholar
  101. Sharrocks AD, Green J & Guest JR (1991) FNR activates and represses transcriptionin vitro. Proc. R. Soc. Lond. B 245: 219–226Google Scholar
  102. Shaw DJ, Rice DW & Guest JR (1983) Homology between CAP and Fnr, a regulator of anaerobic respiration inEscherichia coli. J. Mol. Biol. 166: 241–247Google Scholar
  103. Sirko A, Zehelein E, Freundlich M & Sawers G (1993) Integration host factor is required for anaerobic pyruvate induction of thepfl operon expression inEscherichia coli. J. Bacteriol. 175: 5769–5777Google Scholar
  104. Spangler WJ & Gilmour CM (1966) Biochemistry of nitrate respiration inPseudomonas stutzeri. Aerobic and nitrate respiration routes of carbohydrate catabolism. J. Bacteriol. 91: 245–250Google Scholar
  105. Spiro S & Guest JR (1987b) Activation of thelac operon ofEscherichia coli by a mutant FNR protein. Mol. Microbiol. 1: 53–58Google Scholar
  106. Spiro S & Guest JR (1987a) Regulation and overexpression of thefnr gene ofEscherichia coli. J. Gen. Microbiol. 133: 3279–3288Google Scholar
  107. 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
  108. Spiro S & Guest JR (1990) FNR and its role in oxygen-regulated gene expression inEscherichia coli. FEMS Microbiol. Rev. 75: 399–428Google Scholar
  109. Spiro S & Guest JR (1991) Adaptive responses to oxygen-limitation inEscherichia coli. Trend Biochem. 16: 310–314Google Scholar
  110. Steudel R, Holdt G & Nagorka R (1986) On the autoxidation of aqueous sodium polysulfide. Z. Naturforsch. 41b: 1519–1522Google Scholar
  111. Stewart V (1993) Nitrate regulation of anaerobic respiratory gene expression inEscherichia coli. Molec. Microbiol. 9: 425–434Google Scholar
  112. Stewart V, Parales J & Merkel SM (1989) Structure of genesnarL andnarX of thenar (nitrate reductase) locus inEscherichia coli K-12. J. Bacteriol. 171: 2229–2234Google Scholar
  113. Stock JB, Ninfa AJ & Stock AM (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53: 450–490Google Scholar
  114. Stouthamer A (1988) Bioenergetics and yields with electron acceptors other than oxygen. In: Erickson LE & Fung DYC (Eds) Handbook on anaerobic fermentations (pp 345–435). Marcel Dekker, New YorkGoogle Scholar
  115. Stouthamer AH & van Verseveld HW (1985) Stoichiometry of microbial growth. In: Bull AT & Dalton H (Eds) Comprehensive biotechnology (pp 215–238). Pergamon Press, OxfordGoogle Scholar
  116. Subczynski WK, Hyde JS & Kusumi A (1989) Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proc. Natl. Acad. Sci. USA 86: 4474–4478Google Scholar
  117. Tardat B & Touati D (1993) Iron and oxygen regulation ofEscherichia coli MnSOD expression: competition between the global regulators Fur and ArcA for binding to DNA. Molec. Microbiol. 9: 53–63Google Scholar
  118. Ten Brink B & Konings WN (1980) Generation of an electrochemical proton gradient by lactate efflux in membrane vesicles ofEscherichia coli. Eur. J. Biochem. 111: 59–66Google Scholar
  119. Thauer RK, Jungermann K & Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41: 100–180Google Scholar
  120. Thelander L & Reichard P (1979) Reduction of ribonucleotides. Annu. Rev. Biochem. 48: 133–158Google Scholar
  121. Thelander L, Gräslund A & Thelander M (1983) Continual presence of oxygen and iron required for mammalian ribonucleotide reduction: possible regulation mechanism. Biochem. Biophys. Res. Comm. 111: 859–865Google Scholar
  122. Trageser M & Unden G (1989) Role of cysteine residues and metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration inEscherichia coli. Mol. Microbiol. 3: 593–599Google Scholar
  123. Trageser M, Spiro S, Duchêne A, Kojro E, Fahrenholtz F, Guest JR & Unden G (1990) Isolation of intact FNR protein (Mr 30 000) ofEscherichia coli. Mol. Microbiol. 4: 21–27Google Scholar
  124. Tyson KL, Bell AI, Cole JA & Busby SJW (1993) Definition of nitrite and nitrate response elements at the anaerobically inducibleEscherichia coli nirB promoter: interactions between FNR and NarL. Molec Microbiol. 7: 151–157Google Scholar
  125. Unden G & Guest JR (1985) Isolation and characterization of the FNR protein, the transcriptional regulator of anaerobic electron transport inEscherichia coli. Eur. J. Biochem. 146: 193–199Google Scholar
  126. Unden G & Duchêne A (1987) On the role of cyclic AMP and the FNR protein inEscherichia coli growing anaerobically. Arch. Microbiol. 147: 195–200Google Scholar
  127. Unden G (1988) Differential roles for menaquinone and demethylmenaquinone in anaerobic electron transport ofEscherichia coli and theirfnr-independent expression. Arch. Microbiol. 150: 499–503Google Scholar
  128. Unden G, Trageser M & Duchêne A (1990) Effect of positive redox potentials (>+400 mV) on the expression of anaerobic respiratory enzymes inEscherichia coli. Mol. Microbiol. 4: 315–319Google Scholar
  129. Unden G & Trageser M (1991) Oxygen regulated gene expression inEscherichia coli: control of anaerobic respiration by the FNR protein. Antonie van Leeuwenhoek 59: 65–76Google Scholar
  130. Vasedu van SG, Armarego WLF, Shaw DC, Lilley PE, Dixon NE & Poole RK (1991) Isolation and nucleotide sequence of thehmp gene that encodes a haemoglobin-like protein inEscherichia coli K-12. Mol. Gen. Genet. 226: 49–58Google Scholar
  131. Wagner AFW, Frey M, Neugebauer FA, Schäfer W & Knappe J (1992) The free radical in pyruvate formate-lyase is located on glycine. Proc. Natl. Acad. Sci. USA 89: 996–1000Google Scholar
  132. Walker MS & DeMoss JA (1992) Promoter sequence requirements for Fnr-dependent activation of transcription of thenarGHJI oper-on. Mol. Microbiol. 5: 353–360Google Scholar
  133. Wallace BJ & Young IG (1977b) Role of quinones in electron transport to oxygen and nitrate inEscherichia coli. Biochim. Biophys. Acta 461: 84–100Google Scholar
  134. Weber IT & Steitz TA (1987) Structure of a complex of catabolite gene activator protein and cyclic AMP refined at 2.5 A resolution. J. Mol. Biol. 198: 311–326Google Scholar
  135. Wimpenny JWT & Cole JA (1967) The regulation of metabolism in facultative bacteria. III. The effect of nitrate. Biochim. Biophys. Acta 148: 233: 242Google Scholar
  136. Wissenbach U, Kröger A & Unden G (1990) The specific functions of menaquinone and demethylmenaquinone in anaerobic respiration with fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate byEscherichia coli. Arch. Microbiol. 154: 60–66Google Scholar
  137. Wissenbach U, Ternes D & Unden G (1992) AnEscherichia coli mutant containing only demethylmenaquinone, but no menaquinone: effects on fumarate, DMSO, TMAO and nitrate respiration. Arch. Microbiol. 158: 68–73Google Scholar
  138. Witty JF, Skot L & Revsbeck NP (1987) Direct evidence for changes in the resistance of legume root nodules to O2 diffusion. J. Exp. Bot. 38: 1129–1140Google Scholar
  139. Xu K, Delling J & Elliott T (1992) The genes required for heme synthesis inSalmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J. Bacteriol. 174: 3953–3963Google Scholar
  140. Xu K & Elliott T (1993) An oxygen-dependent coproporphyrinogen oxidase encoded by thehemF gene ofSalmonella typhimurium. J. Bacteriol. 175: 4990–4999Google Scholar
  141. Ziegler DM (1985) Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Ann. Rev. Biochem. 54: 305–329Google Scholar
  142. 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

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • G. Unden
    • 1
  • S. Becker
    • 1
  • J. Bongaerts
    • 1
  • J. Schirawski
    • 1
  • S. Six
    • 1
  1. 1.Institut für Mikrobiologie und WeinforschungJohannes Gutenberg-Universität MainzMainzGermany

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