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Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation

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Abstract

Oxygen is favoured as terminal electron acceptor in aerobic and facultative microorganisms because of its appropriate physical state, satisfactory solubility and its desirable combinations of kinetic and thermodynamic properties. Oxygen is generally reduced by four electrons to yield oxygen, but there are important biological consequences of, and roles for, the partial reduction to superoxide and peroxide. Complex and multiple regulatory networks ensure (i) the utilization of oxygen in preference to other oxidants, (ii) the synthesis of oxygen-consuming enzymes with appropriate properties (particularly affinity for the ligand), and (iii) appropriate cellular protection in the event of oxidative stress. This contribution reviews the terminal respiratory oxidases of selected Gram-negative bacteria and microbial haemoglobin-like proteins.

Recent studies of the cytochromebd-type oxidases ofEscherichia coli andAzotobacter vinelandii suggest that, despite probable similarity at the amino acid level, the reactivities of these oxidases with oxygen are strikingly different. The respiratory protection afforded to nitrogenase in the obligately aerobic diazotrophA. vinelandii by the cytochromebd complex appears to be accompanied by, and may be the result of, a low affinity for oxygen and a high Vmax. The poorly characterized cytochromeo-containing oxidase in this bacterium is not required for respiratory protection. InE. coli, the cytochromebd-type oxidase has a remarkably high affinity for oxygen, consistent with the view that this is an oxygen-scavenging oxidase utilized under microaerobic conditions. The demonstration of substrate (i.e. oxygen) inhibition in this complex suggests a mechanism whereby wasteful electron flux through a non-proton-pumping oxidase is avoided at higher dissolved oxygen tensions. The demonstration of two ligandbinding sites (haemsd andb 595) in oxidases of this type suggests plausible mechanisms for this phenomenon. InE. coli, assembly of the cytochromebd-type oxidase (and of periplasmic cytochromesb andc) requires the presence of an ABC transporter, which may serve to export haem or some “assembly factor' to the periplasm.

There is at least one additional oxygen-consuming protein inE. coli — the flavohaemoglobin encoded by thehmp gene. Globin-like proteins are also widely distributed in other bacteria, fungi and protozoa, but most have unknown functions. The function of HMP and the related chimaeric flavohaemoglobins in other bacteria and yeast is unknown; one of several possibilities for HMP is that its relatively low affinity for oxygen during turnover with NADH as substrate could enable it to function as a sensor of falling (or rising) cytoplasmic oxygen concentrations.

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References

  • 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: 247–252

    PubMed  Google Scholar 

  • Anraku Y (1988) Bacterial electron transport chains. Ann. Rev. Biochem. 57: 101–132

    PubMed  Google Scholar 

  • Appleby CA (1969) Electron transport systems ofRhizobium japonicum II.Rhizobium haemoglobin, cytochromes and oxidases in free-living (cultured) cells. Biochim. Biophys. Acta 172: 88–105

    PubMed  Google Scholar 

  • Appleby CA (1984) Leghaemoglobin andRhizobium respiration. Ann. Rev. Plant Physiol. 35: 443–478

    Google Scholar 

  • Appleby CA, Bogusz D, Dennis ES & Peacock WJ (1988) A role for haemoglobin in all plant roots? Plant Cell Environ. 11: 359–367

    Google Scholar 

  • Appleby CA, Dennis ES & Peacock WJ (1990) A primaeval orgin for plant and animal haemoglobins? Aust. Syst. Bot. 3: 81–89

    Google Scholar 

  • Bebbington KJ & Williams HD (1993) Investigation of the role of thecydD gene product in production of a functional cytochromed oxidase inEscherichia coli. FEMS Microbiol. Lett. 112: 19–24

    PubMed  Google Scholar 

  • Becana M, Salin ML, Ji L & Klucas RV (1991) Flavin-mediated reduction of ferric leghemoglobin from soybean nodules. Planta 183: 575–583

    Google Scholar 

  • Bergerson FJ & Turner GL (1979) Systems utilizing oxygenated leghaemoglobin and myoglobin as sources of free dissolved oxygen at low concentrations for experiments with bacteria. Anal. Biochem. 96: 165–174

    Google Scholar 

  • Bolgiano B, Salmon I, Ingledew WJ & Poole RK (1991) Redox analysis of the cytochromeo-type quinol oxidase complex ofEscherichia coli reveals three redox components. Biochem. J. 274: 723–730

    PubMed  Google Scholar 

  • Calhoun MW, Thomas JW, Hill JJ, Hosler JP, Shapleigh JP, Tecklenburg MMJ, Ferguson-Miller S, Babcock GT, Alben JO & Gennis RB (1993) Identity of the axial ligand of the high-spin heme in cytochrome oxidase. Spectroscopic characterization of mutants in thebo-type oxidase ofEscherichia coli and theaa 3-type oxidase ofRhodobacter sphaeroides. Biochemistry 32: 10905–10911

    PubMed  Google Scholar 

  • Castor LN & Chance B (1959) Photochemical determinations of the oxidases of bacteria. J. Biol. Chem. 234: 1587–1592

    PubMed  Google Scholar 

  • Chance B (1989) Commentary on ‘New methods for the study of the carbon monoxide compounds of respiratory enzymes’. Biochim. Biophys. Acta 1000: 345–347

    PubMed  Google Scholar 

  • Chen L, Liu M-Y, Legall J, Faraleira P, Santos H & Xavier AV (1993) Rubredoxin oxidase, a new flavo-hemo-protein, is the site of oxygen reduction to water by the “strict anaerobe”Desulfovibrio gigas. Biochem. Biophys. Res. Comm. 193: 100–105

    PubMed  Google Scholar 

  • Chepuri V, Lemieux L, Au DCT and Gennis RB (1990) The sequence of thecyo operon indicates substantial structural similarities between the cytochrome-o ubiquinol oxidase ofEscherichia coli and theaa 3-type family of cytochrome-c oxidases. J. Biol. Chem. 265: 11185–11192

    PubMed  Google Scholar 

  • Ciccognani DT, Hughes MN & Poole RK (1992) Carbon monoxide-binding properties of the cytochromebo quinol oxidase complex inEscherichia coli are changed by copper deficiency in continuous culture. FEMS Microbiol. Lett. 94: 1–6

    Google Scholar 

  • Cooper CE, Ioannidis N, D'mello R & Poole RK (1994) Haem, flavin and oxygen interactions in Hmp, a flavohaemoglobin fromEscherichia coli. Biochem. Soc. Trans. (in press)

  • Cotter PA, Chepuri V, Gennis RB & Gunsalus RP (1990) Cytochromeo (cyoABCDE) andd (cydAB) oxidase gene expression is regulated by oxygen, pH, and thefnr gene product. J. Bacteriol. 172: 6333–6338

    PubMed  Google Scholar 

  • Cramm R, Siddiqui RA & Friedrich B (1994) Primary sequence and evidence for a physiological function of the flavohemoprotein ofAlcaligenes eutrophus. J. Biol. Chem. 269: 7349–7354

    PubMed  Google Scholar 

  • D'mello R, Palmer S, Hill S & Poole RK (1994a) The cytochromebd terminal oxidase ofAzotobacter vinelandii: low temperature photodissociation spectrophotometry reveals reactivity of cytochromesb 595 andd with both carbon monoxide and oxygen. FEMS Microbiol. Lett. (submitted)

  • D'mello R, Hill S & Poole RK (1994b) Determination of the oxygen affinities of terminal oxidases inAzotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochromebd is a low-affinity oxidase. Microbiology (in press)

  • Delaney JM & Georgopoulos C (1992) Physical map locations of thetrxB, htrD, cydC, andcydD genes ofEscherichia coli. J. Bacteriol. 174: 3824–3825

    PubMed  Google Scholar 

  • Delaney JM, Wall D & Georgopoulos C (1993) Molecular characterization of theEscherichia coli htrD gene: cloning, sequence, regulation, and involvement with cytochromed oxidase. J. Bacteriol. 175: 166–175

    PubMed  Google Scholar 

  • Dikshit KL & Webster DA (1988) Cloning, characterization and expression of the bacterial globin gene fromVitreoscilla inEscherichia coli. Gene 70: 377–386.

    PubMed  Google Scholar 

  • Dikshit KL, Spaulding D, Braun A & Webster DA (1989) Oxygen inhibition of globin gene transcription and bacterial haemoglobin synthesis inVitreoscilla. J. Gen. Microbiol. 135: 2601–2609

    PubMed  Google Scholar 

  • Dikshit RP, Dikshit KL, Liu Y & Webster DA (1992) The bacterial haemoglobin fromVitreoscilla can support the aerobic growth ofEscherichia coli lacking terminal oxidases. Archiv. Biochem. Biophys. 293: 241–245

    Google Scholar 

  • Eschenbrenner M, Coves J & Fontecave M (1994) Ferric reductases inEscherichia coli: the contribution of the haemoglobin-like protein. Biochem. Biophys. Res. Comm. 198: 127–131

    PubMed  Google Scholar 

  • Fang H, Lin R-J & Gennis RB (1989) Location of heme axial ligands in the cytochromed terminal oxidase complex ofEscherichia coli determined by site-directed mutagenesis. J. Biol. Chem. 264: 8026–8032

    PubMed  Google Scholar 

  • Fath MJ & Kolter R (1993) ABC transporters: bacterial exporters. Microbiol. Rev. 57: 995–1017

    PubMed  Google Scholar 

  • Fu R, Wall JD & Voordouw G (1994) DcrA, ac-type hemecontaining methyl-accepting protein fromDesulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. J. Bacteriol. 176: 344–350

    PubMed  Google Scholar 

  • Georgiou CD, Fang H & Gennis RB (1987) Identification of thecydC locus required for expression of the functional form of the cytochromed terminal oxidase complex inEscherichia coli. J. Bacteriol. 169: 2107–2112

    PubMed  Google Scholar 

  • Gibson QH (1989) Hemoproteins, ligands, and quanta. J. Biol. Chem. 264: 20155–20158

    Google Scholar 

  • Gilles-Gonzalez MA, Ditta GS & Helinski DR (1991) A haemoprotein with kinase activity encoded by the oxgen sensor ofRhizobium meliloti. Nature 350: 170–172

    PubMed  Google Scholar 

  • Goldberg MA, Dunning SP & Bunn HF (1988) Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242: 1412–1415

    PubMed  Google Scholar 

  • Green GN, Fang H, Lin R-J, Newton G, Mather M, Georgiou CD & Gennis RB (1988) The nucleotide sequence of thecyd locus encoding the two subunits of the cytochromed terminal oxidase complex ofEscherichia coli. J. Biol. Chem. 263: 13138–13143

    PubMed  Google Scholar 

  • Green J & Guest JR (1993) Activation of FNR-dependent transcription by iron: an in vitro switch for FNR. FEMS Microbiol. Lett. 113: 219–222

    Google Scholar 

  • Haddock BA & Jones CW (1977) Bacterial respiration. Bacteriol. Rev. 41: 47–99

    PubMed  Google Scholar 

  • Higgins CF (1992) ABC transporters: from microorganisms to man. Ann. Rev. Cell Biol. 8: 67–113

    PubMed  Google Scholar 

  • Hill J, Goswitz VC, Calhoun M, Garcia-Horsman JA, Lemieux L, Alben JO & Gennis RB (1992) Demonstration that thebo-type ubiquinol oxidase ofEscherichia coli contains a heme-copper binuclear center similar to that in cytochromec oxidase and that proper assembly of the binuclear centre requires thecyoE gene product. Biochemistry 31: 11435–11440

    PubMed  Google Scholar 

  • Hill JJ, Alben JO & Gennis RB (1993) Spectroscopic evidence for a heme-heme binuclear center in the cytochromebd ubiquinol oxidase fromEscherichia coli. Proc. Natl. Acad. Sci. USA 90: 5863–5867

    PubMed  Google Scholar 

  • Hill S, Viollet S, Smith AT & Anthony C (1990) Roles for entericd-type cytochrome oxidase in N2 fixation and microaerobiosis. J. Bacteriol. 172: 2071–2078.

    PubMed  Google Scholar 

  • Hussain H, Grove J, Griffiths L, Busby S & Cole JA (1994) A sevengene operon essential for formate-dependent nitrite reduction to ammonia by enteric bacteria. Mol. Microbiol. 12: 153–163

    PubMed  Google Scholar 

  • Ioannidis I, Cooper C & Poole RK (1992) Spectroscopic studies on an oxygen-binding haemoglobin-like flavohaemoprotein fromEscherichia coli. Biochem. J. 288: 649–655

    PubMed  Google Scholar 

  • Iuchi S (1993) Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB ofEscherichia coli. J. Biol. Chem. 268: 23972–23980

    PubMed  Google Scholar 

  • Iuchi S & Lin ECC (1993) Adaptation ofEscherichia coli to redox environments by gene expression. Mol. Microbiol. 9: 9–15

    Google Scholar 

  • Iwaasa H, Takagi T & Shiama K (1990) Protozoan hemoglobin fromTetrahymena pyriformis. Isolation, characterization, and amino acid sequence. J. Biol. Chem. 265: 8603–8609

    Google Scholar 

  • Iwaasa H, Takagi T & Shikama K (1992) Amino acid sequence of yeast hemoglobin. A two-domain structure. J. Mol. Biol. 227: 948–954

    PubMed  Google Scholar 

  • Iwasaki H (1966) Lactate oxidation system inAcetobacter suboxydans, with special reference to carbon monoxide-binding pigment. Plant Cell Physiol. 7: 199–216

    Google Scholar 

  • Jakob W, Webster DA & Kroneck PMH (1992) NADH-dependent methemoglobin reductase from the obligate aerobeVitreoscilla: improved method of purification and reexamination of prosthetic groups. Arch. Biochem. Biophys. 292: 29–33

    PubMed  Google Scholar 

  • Kahlow MA, Zuberi TM, Gennis RB & Loehr TM (1991) Identification of a ferryl intermediate ofEscherichia coli cytochromed terminal oxidase by resonance Raman spectroscopy. Biochemistry 30: 11485–11489

    Google Scholar 

  • Kahn D (1993) Shuffling of an oxygen sensor haem domain. Mol. Microbiol. 8: 786–787

    Google Scholar 

  • Karplus PA, Daniels MJ & Herriott JR (1991) Atomic structure of ferredoxin-NADP+ reductase: prototype for a structurally novel flavoenzyme family. Science 251: 60–66

    PubMed  Google Scholar 

  • Keilin D (1953) Occurrence of haemoglobin in yeast and the supposed stabilization of the oxygenated cytochrome oxidase. Nature 172: 390–393

    PubMed  Google Scholar 

  • Keilin D & Tissières A (1953) Haemoglobin in moulds:Neurospora crassa andPenicillium notatum. Nature 172: 393–394

    PubMed  Google Scholar 

  • Keilin D (1966) The History of Cell Respiration and Cytochrome. Cambridge University Press, Cambridge

    Google Scholar 

  • Kelly MJS, Poole RK, Yates MG & Kennedy C (1990) Cloning and mutagenesis of genes encoding the cytochromebd complex inAzotobacter vinelandii. Mutants deficient in cytochromed are unable to fix nitrogen in air. J. Bacteriol. 172: 6010–6019

    PubMed  Google Scholar 

  • Khosla C & Bailey JE (1988) Heterologous expression of a bacterial haemoglobin improves the growth properties of recombinantEscherichia coli. Nature 331: 633–635

    PubMed  Google Scholar 

  • Khosla C & Bailey JE (1989a) Evidence for partial export ofVitreoscilla hemoglobin into the periplasmic space inEscherichia coli. Implications for protein function. J. Mol. Biol. 210: 79–89

    PubMed  Google Scholar 

  • Khosla C & Bailey JE (1989b) Characterization of the oxygen-dependent promoter of theVitreoscilla hemoglobin gene inEschericia coli. J. Bacteriol. 171: 5995–6004

    PubMed  Google Scholar 

  • Krasnoselskaya I, Arutjunjan AM, Smirnova I, Gennis R & Konstantinov AA (1993) Cyanide-reactive sites in cytochromebd complex fromE. coli. FEBS Lett. 327: 279–283

    PubMed  Google Scholar 

  • Leung D, van der Oost J, Kelly M, Saraste M, Hill S & Poole RK (1994) Mutagenesis of a gene encoding a cytochromeo-like terminal oxidase ofAzotobacter vinelandii: a cytochromeo mutant is aero-tolerant during nitrogen fixation. FEMS Microbiol. Lett. (in press)

  • Light WR & Olson JS (1990) Transmembrane movement of haem. J. Biol. Chem. 265: 15623–15631

    PubMed  Google Scholar 

  • Lorence RM & Gennis RB (1989) Spectroscopic and quantitative analysis of the oxygenated and peroxy states of the purified cytochromed complex ofEscherichia coli. J. Biol. Chem. 264: 7135–7140

    PubMed  Google Scholar 

  • Lorence RM, Koland JG & Gennis RB (1986) Coulometric and spectroscopic analysis of the purified cytochromed complex ofEscherichia coli: evidence for the identification of “cytochromea 1” as cytochromeb 595. Biochemistry 25: 2314–2321

    PubMed  Google Scholar 

  • Minghetti KC, Goswitz VC, Gabriel NE, Hill JJ, Barassi CA, Georgiou CD, Chan SI & Gennis RB (1992) Modified, large-scale purification of the cytochromeo complex (bo-type oxidase) ofEscherichia coli yields a two heme/one copper terminal oxidase with high specific activity. Biochemistry 31: 6917–6924

    PubMed  Google Scholar 

  • Monson EK, Weinstein M, Ditta GS & Helinski DR (1992) The FixL protein ofRhizobium meliloti can be separated into a hemebinding oxygen-sensing domain and a functional C-terminal kinase domain. Proc. Natl. Acad. Sci. USA 89: 4280–4284

    PubMed  Google Scholar 

  • Morgan JE, Verkhovsky MI, Puustinen A & Wikström M (1993) Intramolecular electron transfer in cytochromeo ofEscherichia coli: events following the photolysis of fully and partially reduced CO-bound forms of thebo 3 andoo 3 enzymes. Biochemistry 32: 11413–11418

    PubMed  Google Scholar 

  • Moshiri F, Chawla A & Maier RJ (1991) Cloning, characterization, and expression inEscherichia coli of the genes encoding the cytochromed oxidase complex fromAzotobacter vinelandii. J. Bacteriol. 173: 6230–6241

    Google Scholar 

  • Orii Y, Ioannidis N & Poole RK (1992) The oxygenated flavohaemoglobin fromEscherichia coli: evidence from photodissociation and rapid-scan studies for two oxygenated forms. Biochem. Biophys. Res. Commun. 187: 94–100

    PubMed  Google Scholar 

  • Oshino R, Oshino N, Chance B & Hagihara B (1973a) Studies on yeast hemoglobin. The properties of yeast hemoglobin and its physiological function in the cell. Eur. J. Biochem. 35: 23–33

    PubMed  Google Scholar 

  • Oshino R, Asakura T, Takio K, Oshino N, Chance B & Hagihara B (1973b) Purification and molecular properties of yeast hemoglobin. Eur. J. Biochem. 39: 581–590

    PubMed  Google Scholar 

  • Perutz MF (1986) A bacterial haemoglobin. Nature 322: 405

    Google Scholar 

  • Poole RK (1983) Bacterial cytochrome oxidases: a structurally and functionally diverse group of electron transfer proteins. Biochim. Biophys. Acta 726: 205–283

    PubMed  Google Scholar 

  • Poole RK (1988) Bacterial cytochrome oxidases. In: Anthony C (ed) Bacterial Energy Transduction (pp 231–291) Academic Press, London

    Google Scholar 

  • Poole RK & Ingledew WJ (1987)Escherichia coli andSalmonella typhimurium. In: Ingraham JL, Low KB, Magasanick B, Schaechter M and Umbarger H (eds) Cellular and Molecular Biology, Vol. 1 (pp 170–200) American Society for Microbiology, Washington, DC

    Google Scholar 

  • Poole RK & Williams HD (1988). Formation of the 680 nmabsorbing form of the cytochromebd oxidase complex ofEscherichia coli by reaction of hydrogen peroxide with the oxidized form. FEBS Lett. 231: 243–246

    PubMed  Google Scholar 

  • Poole RK, Waring AJ & Chance B (1979) The reaction of cytochromeo inEscherichia coli with oxygen. Low-temperature kinetic and spectral studies. Biochem. J. 184: 379–389

    Google Scholar 

  • Poole RK, Scott RI & Chance B (1981) The light-reversible binding of carbon monoxide to cytochromea 1 inEscherichia coli K12. J. Gen. Microbiol. 125: 431–438

    PubMed  Google Scholar 

  • Poole RK, Sivaram A, Salmon I & Chance B (1982) Photolysis at very low temperatures of CO-liganded cytochrome oxidase (cytochromed) in oxygen-limitedEscherichia coli. FEBS Lett. 141: 237–241

    PubMed  Google Scholar 

  • Poole RK, Kumar C, Salmon I & Chance B (1983) The 650 nm chromophore inEscherichia coli is an “oxy” — or oxygenated compound, not the oxidized form of cytochrome oxidased: a hypothesis. J. Gen. Microbiol. 129: 1335–1344

    PubMed  Google Scholar 

  • Poole RK, Williams HD, Downie JA & Gibson F (1989) Mutations affecting the cytochromed-containing oxidase complex ofEscherichia coli K12: Identification and mapping of a fourth locus,cydD. J. Gen. Microbiol. 135: 1865–1874

    PubMed  Google Scholar 

  • Poole RK, Hatch L, Cleeter M, Gibson F, Cox GB & Wu G (1993) Cytochromebd biosynthesis inEscherichia coli: the sequences of thecydC andcydD genes suggest that they encode the components of an ABC membrane transporter. Mol. Microbiol. 10: 421–430

    PubMed  Google Scholar 

  • Poole RK, Salmon I & Chance B (1994a) The high-spin cytochromeo′ component of the cytochromebo-type quinol oxidase in membranes fromEscherichia coli: formation of the primary oxygenated species at low temperature is characterized by a slow ‘on’ rate and low dissociation constant. Microbiology (in press)

  • Poole RK, Gibson F & Wu G (1994b) ThecydD gene product, component of a heterodimeric ABC transporter, is required for assembly of periplasmic cytochromec and of cytochromebd inEscherichia coli. FEMS Microbiol. Lett. 117: 217–224

    PubMed  Google Scholar 

  • Poole RK, D'mello R, Hill, S. Ioannidis I, Leung D & Wu G (1994c) The oxygen reactivity of bacterial respiratory haemoproteins: oxidases and globins. Biochim. Biophys. Acta (in press)

  • Poole RK, Ioannidis N & Orii Y (1994d) Reactions of theEscherichia coli flavohaemoglobin (Hmp) with oxygen and reduced nicotinamide adenine dinucleotide. Evidence for oxygen switching of flavin oxidoreduction and a mechanism for oxygen sensing. Proc. Roy. Soc. Ser. B 255: 251–258

    Google Scholar 

  • Potts M, Angeloni SV, Ebel RE & Bassam D (1992) Myoglobin in a cyanobacterium. Science 256: 1690–1692

    PubMed  Google Scholar 

  • Preisig O, Anthamatten D & Hennecke H (1993) Genes for a microaerobically induced oxidase complex inBradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. 90: 3309–3313

    PubMed  Google Scholar 

  • Probst I, Wolf G, Schlegel HG & Fischer G (1979) An oxygen-binding flavohaemoprotein fromAlcaligenes eutrophus. Biochim. Biophys. Acta 576: 471–478

    PubMed  Google Scholar 

  • Puustinen A & Wikström M (1991) The haem groups of cytochromeo fromEscherichia coli. Proc. Natl. Acad. Sci. USA 88: 6122–6126

    Google Scholar 

  • Puustinen A, Finel M, Haltia T, Gennis RB & Wikström M (1991) Properties of the two terminal oxidases fromEscherichia coli. Biochemistry 30: 3936–3942

    PubMed  Google Scholar 

  • Puustinen A, Morgan JE, Verkhovsky M, Thomas J W, Gennis RB & Wikström M (1992) The low-spin heme site of cytochromeo fromEscherichia coli is promiscuous with respect to heme type. Biochemistry 31: 10363–10369

    PubMed  Google Scholar 

  • Saiki K, Mogi T & Anraku Y (1992) Heme O biosynthesis inEscherichia coli: thecyoE gene in the cytochromebo operon encodes a protoheme IX farnesyltransferase. Biochem. Biophys. Res. Comm. 189: 1491–1497

    Google Scholar 

  • Salerno JC, Bolgiano B, Poole RK, Gennis RB & Ingledew WJ (1990). Heme-copper and heme-heme interactions in the cytochromebo-containing quinol oxidase ofEscherichia coli. J. Biol. Chem. 265: 4364–4368

    PubMed  Google Scholar 

  • Saraste M (1994) Structure and evolution of cytochrome oxidase. Antonie van Leeuwenhoek (this issue) 65: 285–287

    Google Scholar 

  • Siegele DA & Kolter R (1993) Isolation and characterization of anEscherichia coli mutant defective in resuming growth after starvation. Genes Dev. 7: 2629–2640

    PubMed  Google Scholar 

  • Stewart V (1993) Nitrate regulation of anaerobic respiratory gene expression inEscherichia coli. Mol. Microbiol. 9: 425–434

    Google Scholar 

  • Svensson M & Nilsson T (1993) Flow-flash study of the reaction between cytochromebo and oxygen. Biochemistry 32: 5442–5447

    PubMed  Google Scholar 

  • Takagi T (1993) Hemoglobins from single-celled organisms. Curr. Opin. Struct. Biol. 3: 413–418

    Google Scholar 

  • Thöny-Meyer L, Ritz & Hennecke H (1994) Cytochromec biogenesis in bacteria: a possible pathway begins to emerge. Mol. Microbiol. 12: 1–9

    PubMed  Google Scholar 

  • Timkovich R, Cork MS, Gennis RB & Johnson PY (1985) Proposed structure of hemed, a prosthetic group of bacterial terminal oxidases. J. Am. Chem. Soc. 107: 6069–6075

    Google Scholar 

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

    PubMed  Google Scholar 

  • van der Oost J, de Boer APN, de Gier J-WL, Zumft WG, Stouthamer AH & van Spanning R (1994) The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol. Lett. (in press)

  • Vasudevan 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: 49–58

    PubMed  Google Scholar 

  • Verhoeven W (1956) Some remarks on nitrate and nitrite metabolism in microorganisms. In: McElroy WD and Glass B (eds) Inorganic Nitrogen Metabolism: Function of Metallo-Flavoproteins (pp61–86) Johns Hopkins Press, Baltimore

    Google Scholar 

  • Wakabayashi S, Matsubara H & Webster DA (1986) Primary sequence of a dimeric bacterial haemoglobin fromVitreoscilla. Nature 322: 481–483

    PubMed  Google Scholar 

  • Webster DA (1987) Structure and function of bacterial hemoglobin and related proteins. In: Eichhorn GL and Marzilli LG (eds) Advances in Inorganic Chemistry, Vol 7, Haem Proteins (pp 245–265) Elsevier, New York

    Google Scholar 

  • Wittenberg JB & Wittenberg BA (1990) Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annu. Rev. Biophys. Biophys. Chem. 19: 217–241

    PubMed  Google Scholar 

  • Wood PM (1984) Bacterial proteins with CO-bindingb- orc-type haem. Functions and absorption spectroscopy. Biochim. Biophys. Acta 768: 293–317

    Google Scholar 

  • Wu G, Williams HD, Gibson F & Poole RK (1993) Mutants ofEscherichia coli affected in respiration: the cloning and nucleotide sequence ofubiA, encoding the membrane-boundp-hydroxybenzoate:octaprenyl transferase. J. Gen. Microbiol. 139: 1795–1805

    PubMed  Google Scholar 

  • Xu F, Quandt KS & Hultquist DE (1992) Characterization of NADPH-dependent methemoglobin reductase as a heme-binding protein present in erythrocytes and liver. Proc. Natl. Acad. Sci. USA 89: 2130–2134

    PubMed  Google Scholar 

  • Yamauchi K, Ochiai T & Usuki I (1992) The unique structure of theParamecium caudatum hemoglobin gene: the presence of one intron in the middle of the coding region. Biochim. Biophys. Acta 1171: 81–87

    PubMed  Google Scholar 

  • Youngson C, Nurse C, Yeger H & Cutz E (1993) Oxygen sensing in airway chemoreceptors. Nature 365: 153–155

    PubMed  Google Scholar 

  • Zhu H & Riggs AF (1992) Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. Proc. Natl. Acad. Sci. USA 89: 5015–5019

    PubMed  Google Scholar 

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    Robert K. Poole

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(until October 1994: Section of Microbiology, Wing Hall, Cornell University, Ithaca, NY 14853-8101, USA)

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Poole, R.K. Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation. Antonie van Leeuwenhoek 65, 289–310 (1994). https://doi.org/10.1007/BF00872215

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