1887

Abstract

An knockout mutant has been constructed using a gene replacement method and verified using both Southern hybridization and PCR. The mutant, which was unable to synthesize ubiquinone (Q), showed severely diminished growth yields aerobically but not anaerobically with either nitrate or fumarate as terminal electron acceptors. Low oxygen uptake rates were demonstrated in membrane preparations using either NADH or lactate as substrates. However, these rates were greatly stimulated by the addition of ubiquinone-1 (Q-1). The rate of electron transfer to those oxidase components observable by photodissociation of their CO complexes was studied at sub-zero temperatures. In the mutant, the reduced form of haemoproteins - predominantly cytochrome -was reoxidized significantly faster in the presence of oxygen than in a Ubi strain, indicating the absence of Q as electron donor. Continuous multiple-wavelength recordings of the oxidoreduction state of cytochrome(s) during steady-state respiration showed greater reduction in membranes from the mutant than in wild-type membranes. A scheme for the respiratory electron-transfer chain in is proposed, in which Q functions downstream of cytochrome(s) .

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1998-02-01
2024-10-12
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References

  1. Au D. C.-T., Green G. N., Gennis R. B. 1984; Role of quinones in the branch of the Escherichia coli respiratory chain that terminates in cytochrome o . J Bacteriol 157:122–125
    [Google Scholar]
  2. Brito F., DeMoss i. A., Dubourdieu M. 1995; Isolation and identification of menaquinone-9 from purified nitrate reductase of Escherichia coli . J Bacteriol 177:3728–3735
    [Google Scholar]
  3. Chance B., Williams G. R. 1956 The respiratory chain and oxidative phosphorylation.. In Advances in Enzymology and Related Subjects of Biochemistry vol 17 pp 65–134 Edited by Nord F. F. New York: Interscience;
    [Google Scholar]
  4. Chance B., Graham N., Legallais V. 1975a; Low temperature trapping method for cytochrome oxidase oxygen intermediates.. Anal Biochem 67:552–579
    [Google Scholar]
  5. Chance B., Saronio C., Leigh J. S. 1975b; Functional intermediates in the reaction of membrane-bound cytochrome oxidase with oxygen.. J Biol Chem 250:9226–9237
    [Google Scholar]
  6. Cox G., B, Newton N. A., Gibson F., Snoswell A. M., Hamilton J. A. 1970; The function of ubiquinone in Escherichia coli . Biochem J 117:551–562
    [Google Scholar]
  7. Daniels D. L., Plunkett G., Burland V., Blattner F. R. 1992; Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes.. Science 257:771–778
    [Google Scholar]
  8. D'mello R., Hill S., Poole R. K. 1994; Determination of the oxygen affinities of terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyo- globin: cytochrome bd is a low-affinity oxidase.. Microbiology 140:1395–1402
    [Google Scholar]
  9. D'mello R., Hill S., Poole R. K. 1996; The cytochrome bd quinol oxidase in Escherichia coli has an extremely high affinity for oxygen and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition.. Microbiology 142:755–763
    [Google Scholar]
  10. Downie J. A., Cox G. B. 1978; Sequence of b cytochromes relative to ubiquinone in the electron transport chain of Escherichia coli . J Bacteriol 133:477–484
    [Google Scholar]
  11. Friedrich T. 10 other authors 1994; Two binding sites of inhibitors in NADH:ubiquinone oxidoreductase (complex I). Relationship of one site with the ubiquinone-binding site of bacterial glucose: ubiquinone oxidoreductase.. Eur J Biochem 219:691–698
    [Google Scholar]
  12. Gennis R. B. 1987; The cytochromes of Escherichia coli . FEMS Microbiol Rev 46:387–399
    [Google Scholar]
  13. Gennis R. B., Stewart V. 1996 Respiration.. In Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd edn, pp 217–261 Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  14. Gibson F. 1973; Chemical and genetic studies on the biosynthesis of ubiquinone by Escherichia coli . Biochem Soc Trans 1:317–326
    [Google Scholar]
  15. Green J., Guest J. R. 1994; Regulation of transcription at the ndh promoter of Escherichia coli by FNR and novel factors.. Mol Microbiol 12:433–444
    [Google Scholar]
  16. Haddock B. A., Downie J. A., Garland P. B. 1976; Kinetic characterization of the membrane-bound cytochromes of Escherichia coli grown under a variety of conditions by using a stopped-flow dual-wavelength spectrophotometer.. Biochem J 154:285–294
    [Google Scholar]
  17. Hamilton C. M., Aldea M., Washburn B. K., Babitzke P., Kushner S. R. 1989; New method for generating deletions and gene replacements in Escherichia coli . J Bacteriol 171:4617–4622
    [Google Scholar]
  18. Hsu A. Y., Poon W. W., Shepherd J., K, Myles D. C., Clarke C. F. 1996; Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O-methylation steps in ubiquinone biosynthesis.. Biochemistry 35:9797–9806
    [Google Scholar]
  19. Ingledew W. J., Poole R. K. 1984; The respiratory chains of Escherichia coli . Microbiol Rev 48:221–271
    [Google Scholar]
  20. Ingledew W. J., Ohnishi T., Salerno J. C. 1995; Studies on a stabilisation of ubisemiquinone by Escherichia coli quinol oxidase, cytochrome bo . Eur J Biochem 227:903–908
    [Google Scholar]
  21. Kita K., Anraku Y. 1981; Composition and sequence of b cytochromes in the respiratory chain of aerobically grown Escherichia coli K-12 in the early exponential phase.. Biochem Int 2:105–112
    [Google Scholar]
  22. Kita K., Yamato I., Anraku Y. 1978; Purification and properties of cytochrome b556 in the respiratory chain of aerobically grown Escherichia coli K12.. J Biol Chem 253:8910–8915
    [Google Scholar]
  23. Lee P. T., Hsu A. Y., Ha H. T., Clarke C. F. 1997; A C-methyltransferase involved in both ubiquinone and menaquinone biosynthesis: isolation and identification of the Escherichia coli ubiE gene.. J Bacteriol 179:1748–1754
    [Google Scholar]
  24. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual 2nd edn Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  25. Markwell M. A. K., Haas S. M., Bieber L. L., Tolbert N. E. 1978; A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.. Anal Biochem 87:206–210
    [Google Scholar]
  26. Meganathan R. 1996 Biosynthesis of the isoprenoid quinones menaquinone (vitamin K2) and ubiquinone (coenzyme Q).. In Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd edn, pp 642–656 Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  27. Murakami H., Kita K., Anraku Y. 1984; Cloning of cybB, the gene for cytochrome b561 of Escherichia coli . Mol Gen Genet 198:1–6
    [Google Scholar]
  28. Murakami H., Kita K., Oya H., Anraku Y. 1985; The Escherichia coli cytochrome b556 gene, cybA, is assignable as sdhC in the succinate dehydrogenase gene cluster.. FEMS Microbiol Lett 30:307–311
    [Google Scholar]
  29. Murakami H., Kita K., Anraku Y. 1986; Purification and properties of a diheme cytochrome b 561 of the Escherichia coli respiratory chain.. J Biol Chem 261:548–551
    [Google Scholar]
  30. Nakahigashi K., Miyamoto K., Nishimura K., Inokuchi H. 1992; Isolation and characterization of a light-sensitive mutant of Escherichia coli K-12 with a mutation in a gene that is required for the biosynthesis of ubiquinone.. J Bacteriol 174:7352–7359
    [Google Scholar]
  31. Nonet M. L., Marvel C. C., Tolan D. R. 1987; The hisT-purF region of the Escherichia coli K-12 chromosome. Identification of additional genes of the hisT and purF operons.. J Biol Chem 262:12209–12217
    [Google Scholar]
  32. Okada K., Minehara M., Zhu X., Suzuki K., Nakagawa T., Matsuda H., Kawamukai M. 1997; The ispB gene encoding octaprenyl diphosphate synthase is essential for growth of Escherichia coli . J Bacteriol 179:3058–3060
    [Google Scholar]
  33. Poole R. K. 1977; The influence of growth substrate and capacity for oxidative phosphorylation on respiratory oscillations in synchronous cultures of Escherichia coli K-12.. J Gen Microbiol 99:369–377
    [Google Scholar]
  34. Poole R. K. 1983; Bacterial cytochrome oxidases: a structurally and functionally diverse group of electron transfer proteins.. Biochim Biophys Acta 726:205–243
    [Google Scholar]
  35. Poole R. K., Chance B. 1981; The reaction of cytochrome o in Escherichia coli K12 with oxygen. Evidence for a spectrally and kinetically distinct form of cytochrome o in cells from oxygen- limited cultures.. J Gen Microbiol 126:277–287
    [Google Scholar]
  36. Poole R. K., Sivaram A., Salmon I., Chance B. 1982; Photolysis at very low temperature of CO-ligated cytochrome oxidase (cytochrome d) in oxygen-limited Escherichia coli . FEBS Lett 141:237–241
    [Google Scholar]
  37. Poole R. K., Williams H. D., Downie J. A., Gibson F. 1989; Mutations affecting the cytochrome d-containing oxidase complex of Escherichia coli K12: identification and mapping of a fourth locus, cydD . J Gen Microbiol 135:1865–1874
    [Google Scholar]
  38. Poole R. K., loannidis N., Yutaka O. 1994; Reactions of the Escherichia coli flavohaemoglobin (Hmp) with oxygen and reduced nicotinamide adenine dinucleotide: evidence for oxygen switching of flavin oxidoreduction and a mechanism for oxygen sensing.. Proc R Soc Lond 255:251–258
    [Google Scholar]
  39. Puustinen A., Verkhovsky M. I., Morgan J. E., Belevich N. P., Wikstrttm M. 1996; Reaction of the Escherichia coli quinol oxidase cytochrome bo. with dioxygen: the role of a bound ubiquinone molecule.. Proc Natl Acad Sci USA 93:1545–1548
    [Google Scholar]
  40. Sato-Watanabe M., Mogi T., Ogura T., Kitagawa T., Miyoshi H., Iwamura H., Anraku Y. 1994; Identification of a novel quinone-binding site in the cytochrome bo complex from Escherichia coli . J Biol Chem 269:28908–28912
    [Google Scholar]
  41. Sato-Watanabe M., Itoh S., Mogi T., Matsuura K., Miyoshi H., Anraku Y. 1995; Stabilization of a semiquinone radical at the high-affinity quinone-binding site (QH) of the Escherichia coli bo- type ubiquinol oxidase.. FEBS 374:265–269
    [Google Scholar]
  42. Spyrou G., Haggard-Ljungquist E., Krook M., Jornvall H., Nusson E., Reichard P. 1991; Characterisation of the flavin reductase gene (fre) of Escherichia coli and construction of a plasmid for overproduction of the enzyme.. J Bacteriol 173:3673–3679
    [Google Scholar]
  43. Stewart V., Parales J. 1988; Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12 . J Bacteriol 170:1589–1597
    [Google Scholar]
  44. Sturr M. G., Krulwich T. A., Hicks D. B. 1996; Purification of a cytochrome bd terminal oxidase encoded by the Escherichia coli app locus from a A cyo A cyd strain complemented by genes from Bacillus firmus OF4.. J Bacteriol 176:1742–1749
    [Google Scholar]
  45. Trower M. K. 1993; PCR cloning, sequence analysis and expression of the cybC genes encoding soluble cytochrome b-562 from Escherichia coli B strain OP7 and K Strain NM522.. Biochim Biophys Acta 1143:109–111
    [Google Scholar]
  46. Wallace B J., Young I. G. 1977; Role of quinones in electron transport to oxygen and nitrate in Escherichia coli. Studies with a ubiAr menAC double quinone mutant.. Biochim Biophys Acta 461:84–100
    [Google Scholar]
  47. Weidner U., Geier S., Ptock A., Friedrich T., Leif H., Weiss H. 1993; The gene locus of the proton-translocating NADH: ubiquinone oxideoreductase in Escherichia coli . J Mol Biol 233:109–122
    [Google Scholar]
  48. Westenberg D. J., Gunsalus R. P., Ackrell B. A. C., Sices H., Cecchini G. 1993; Escherichia coli fumarate reductase frdC and frdD mutants. Identification of amino acid residues involved in catalytic activity with quinones.. J Biol Chem 268:815–822
    [Google Scholar]
  49. Williams H. D., Poole R. K. 1987; The cytochromes of Acetobacter pasteurianus NCIB 6428. Evidence of a role for acytochrome a1-like haemoprotein in electron transfer to cytochrome oxidase d . J Gen Microbiol 133:2461–2472
    [Google Scholar]
  50. Wu G., Williams H. D., Zamanian M., Gibson F., Poole R. K. 1992; Isolation and characterisation of Escherichia coli mutants affected in aerobic respiration: the cloning and nucleotide sequence of ubiG . J Gen Microbiol 138:2101–2112
    [Google Scholar]
  51. Wu G., Williams H. D., Gibson F., Poole R. K. 1993; Mutants of Escherichia coli affected in respiration: the cloning and nucleotide sequence of ubiA, encoding the membrane-bound p- hydroxybenzoate:octaprenyltransferase.. J Gen Microbiol 139:1795–1805
    [Google Scholar]
  52. Yamato I., Nakamura H., Murakami H., Anraku Y. 1988; Mapping and disruption of the cybB gene coding for cytochrome b5%l in Escherichia coli . FEMS Microbiol Lett 56:21–28
    [Google Scholar]
  53. Zhu X., Yuasa M., Okada K., Suzuki K., Nakagawa T., Kawamukai M., Matsuda H. 1995; Production of ubiquinone in Escherichia coli by expression of various genes responsible for ubiquinone biosynthesis.. J Ferment Bioeng 79:493–495
    [Google Scholar]
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