1887

Abstract

Summary: Cytochrome has been implicated in having an important role in microaerobic nitrogen fixation in the enteric bacterium , where it is expressed under all conditions that permit diazotrophy. In this paper the sequence of the genes encoding this terminal oxidase () of and the characterization of a mutant are reported. The deduced amino acid sequences support the proposal that His 19, His 186 and Met 393 provide three of the four axial ligands to the Fe of the three haems in the oxidase complex. The nitrogen-fixing ability of the mutant was severely impaired in the presence of low concentrations of oxygen compared with the wild-type bacterium. Only the wild-type organism was capable of microaerobic nitrogenase activity supported by fermentation products. It is proposed that formate dehydrogenase-O may be involved in supplying electrons to a respiratory chain terminated by the -type oxidase, which would remove inhibitory oxygen and supply ATP for nitrogenase activity.

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1997-08-01
2024-04-19
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Anraku Y., Gennis R. B. 1987; The aerobic respiratory chain of Escherichia coli. . Trends Biochem Sci 12:262–266
    [Google Scholar]
  3. Bishop P. E., Premakumar R. 1992; Alternative nitrogen fixation systems. . In Biological Nitrogen Fixation pp. 736–762 . Edited by Stacey G., Burris R. H., Evans H. J. New York & London: Chapman & Hall;
    [Google Scholar]
  4. Bock A., Sawers G. 1996; Fermentation. . In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology 2nd edn, pp 262–282 . Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  5. Cannon F. C. 1984; Genetic studies with diazotrophs. . In Methods for Evaluating Biological Nitrogen Fixation pp. 367–413 . Edited by Bergersen F. J. Chichester: Wiley;
    [Google Scholar]
  6. Dassa J., Fsihi H., Marck C., Dion M., Kieffer-bontemps M., Boquet P. L. 1991; A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA). . Mol Gen Genet 229:341–352
    [Google Scholar]
  7. D'mello R., Hill S., Poole R. K. 1994; Determination of the oxygen affinities of the terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochrome bd is a low-affinity oxidase. Microbiology 140:1395–1402
    [Google Scholar]
  8. D'mello R., Hill S., Poole R. K. 1996; The cytochrome bd quinol oxidase in E. coli has an extremely high oxygen affinity: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142:755–763
    [Google Scholar]
  9. D'mello R., Purchase D., Poole R. K., Hill S. 1997; Expression and content of terminal oxidases in Azotobacter vinelandii grown with excess NH+ 4 are modulated by O2 supply. Microbiology 143:231–237
    [Google Scholar]
  10. Dueweke T. J., Gennis R. B. 1990; Epitopes of monoclonal antibodies which inhibit ubiquinol oxidase activity of Escherichia coli cytochrome d complex localize functional domain. J Biol Chem 265:4273–4277
    [Google Scholar]
  11. Dueweke T. J., Gennis R. B. 1991; Proteolysis of the cytochrome d complex with trypsin and chymotrypsin localizes a quinol oxidase domain. Biochemistry 30:3401–3406
    [Google Scholar]
  12. Fang H., Gennis R. B. 1993; Identification of the transcriptional start site of the cyd operon from Escherichia coli. . FEMS Microbiol Lett 108:237–242
    [Google Scholar]
  13. Fang H., Lin R.-J., Gennis R. B. 1989; Location of heme axial ligands in the cytochrome d terminal oxidase complex of Escherichia coli determined by site-directed mutagenesis. J Biol Chem 264:8026–8032
    [Google Scholar]
  14. Fleischmann J. and others 1995; Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512
    [Google Scholar]
  15. Goldman B. S., Gabbert K. K., Kranz R. G. 1996; The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178:6348–6351
    [Google Scholar]
  16. Green G. N., Kranz J. E., Gennis R. B. 1984; Cloning of the cyd gene locus coding for the cytochrome d complex of Escherichia coli. . J Bacteriol 32:99–106
    [Google Scholar]
  17. Green G. N., Fang H., Lin R.-J., Newton G., Mathers M., Georgiou C. D., Gennis R. B. 1988; The nucleotide sequence of the cyd locus encoding the two subunits of the cytochrome d terminal oxidase complex of Escherichia coli. . J Biol Chem 263:13138–13143
    [Google Scholar]
  18. Hill S. 1976a; Influence of the atmospheric oxygen concentration on acetylene reduction and efficiency of nitrogen fixation in intact Klebsiella pneumoniae. . J Gen Microbiol 93:335–345
    [Google Scholar]
  19. Hill S. 1976b; The apparent ATP requirement for nitrogen fixation in growing Klebsiella pneumoniae. . J Gen Microbiol 95:297–312
    [Google Scholar]
  20. Hill S. 1992; Physiology of nitrogen fixation in free-living heterotrophs. . In Biological Nitrogen Fixation pp. 87–134 . Edited by Stacey G., Burris R. H., Evans H. J. New York & London: Chapman & Hall;
    [Google Scholar]
  21. Hill S., Kavanagh E. 1980; Roles of nifF and nifJ gene products in electron transfer to nitrogenase in Klebsiella pneumoniae. . J Bacteriol 141:470–475
    [Google Scholar]
  22. Hill S., Turner G. L., Bergersen F. J. 1984; Synthesis and activity of nitrogenase in Klebsiella pneumoniae exposed to low concentration of oxygen. J Gen Microbiol 130:1061–1067
    [Google Scholar]
  23. Hill S., Viollet S., Smith A. T., Anthony C. 1990; Roles for enteric d-type cytochrome oxidase in nitrogen fixation and microaerobiosis. J Bacteriol 172:2071–2078
    [Google Scholar]
  24. Hill S., Kavanagh E., Munn J. A., Kahindi J., Campbell F., Yates M. G., D'mello R., Poole R. K. 1995; Physiology of N2 fixation relating to N, O2 and H2 status in free-living heterotrophs. . In Nitrogen Fixation with Non-legumes pp. 15–25 . Edited by Hegazi N. A., Fayez M., Monid M. Cairo: The American University in Cairo Press;
    [Google Scholar]
  25. Jünemann S., Butterworth P. J., Wrigglesworth J. M. 1995; A suggested mechanism for the catalytic cycle of cytochrome bd terminal oxidase based on kinetic analysis. Biochemistry 34:14861–14867
    [Google Scholar]
  26. Juty N. S., Hill S., Anthony C. 1995; Isolation and characterization of a cyd mutant of Klebsiella pneumoniae. . In Nitrogen Fixation: Fundamentals and Applications. Proceedings of the 10th International Congress on Nitrogen Fixation, St Petersburg, Russia p. 216. Edited by Tikhonovich I. A., Provorov N. A., Romanov V. I., Newton W. E. Dordrecht: Kluwer Academic;
    [Google Scholar]
  27. Kaneko T. and others 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136
    [Google Scholar]
  28. Kavanagh E. P., Hill S. 1990; The automatic maintenance of low dissolved oxygen using a photobacterial oxygen sensor for the study of microaerobiosis. J Appl Bacteriol 69:539–549
    [Google Scholar]
  29. Kaysser T. M., Ghaim J. B., Georgiou C., Gennis R. B. 1995; Methionine-393 is an axial ligand of the heme b-558 component of the cytochrome bd ubiquinol oxidase from E. . coli. Biochemistry 34:13491–13501
    [Google Scholar]
  30. Kelly M. J. S., Poole R. K., Yates M. G., Kennedy C. 1990; Cloning and mutagenesis of the genes encoding the cytochrome bd terminal oxidase complex in A. vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air. J Bacteriol 172:6010–6019
    [Google Scholar]
  31. Kita K., Konishi K., Anraku Y. 1984; Terminal oxidases of the Escherichia coli aerobic respiratory chain. II. Purification and properties of the cytochrome b 558 –d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J Biol Chem 259:3375–3381
    [Google Scholar]
  32. Kolonay J. F., Moshiri F., Gennis R. B., Kaysser T. M., Maier R. J. 1994; Purification and characterisation of the cytochrome bd complex from Azotobacer vinelandii: comparison to the complex from Escherichia coli. . J Bacteriol 176:4177–4181
    [Google Scholar]
  33. Moshiri F., Chawla A., Maier R. J. 1991a; Cloning, characterization, and expression in Escherichia coli of the genes encoding the cytochrome d oxidase complex from Azotobacter vinelandii. . J Bacteriol 173:6230–6241
    [Google Scholar]
  34. Moshiri F., Smith E. G., Taormino J. P., Maier R. J. 1991b; Transcriptional regulation of cytochrome d in nitrogen-fixing Azotobacter vinelandii. . J Biol Chem 266:32169–23174
    [Google Scholar]
  35. Paul W., Merrick M. 1989; The roles of the nifW, nifZ and nifM genes of Klebsiella pneumoniae in nitrogenase biosynthesis. Eur J Biochem 178:675–682
    [Google Scholar]
  36. Pearson W. R., Lipman D. J. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448
    [Google Scholar]
  37. Poole R. K., Waring A. J., Chance B. 1979; The reactions of cytochrome o with oxygen: low temperature and spectral studies. Biochem J 184:369–389
    [Google Scholar]
  38. Poste E., Kleiner D., Oelze J. 1983; Whole cell respiration and nitrogenase activities in Azotobacter vinelandii growing in an oxygen controlled continuous culture. Arch Microbiol 134:68–72
    [Google Scholar]
  39. Postgate J. R., Dixon R., Hill S., Kent H. 1987; Nif genes in alien backgrounds. Philos Trans R Soc Lond Biol Sci 317:227–241
    [Google Scholar]
  40. Prentki P., Kirsch H. 1984; In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313
    [Google Scholar]
  41. Robson R. L., Chesshyre J. A., Wheeler C., Jones R., Woodley P. R., Postgate J. R. 1984; Genome size and complexity in Azotobacter chroococcum. . J Gen Microbiol 130:1603–1612
    [Google Scholar]
  42. Rost B., Casadio R., Fariselli P., Sander C. 1995; Transmembrane helices predicted at 95% accuracy. Protein Sci 4:521–533
    [Google Scholar]
  43. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  44. Sawers G. 1994; The hydrogenases and formate dehydrogenases of E. . coli. Antonie Leeuwenhoek 66:57–88
    [Google Scholar]
  45. Shah V. K., Stacey G., Brill W. J. 1983; Electron transport to nitrogenase: purification and characterisation of pyruvate: flavodoxin oxidoreductase, the nifJ product. J Biol Chem 258:12064–12068
    [Google Scholar]
  46. Smith A., Hill S., Anthony C. 1990; The purification, characterization and role of the d-type cytochrome oxidase of Klebsiella pneumonaie during nitrogen fixation. J Gen Microbiol 136:171–180
    [Google Scholar]
  47. Sprent J. I., Sprent P. 1990 Nitrogen Fixing Organisms London & New York: Chapman & Hall;
    [Google Scholar]
  48. 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 ∆cyo ∆cyd strain complemented by genes from Bacillus firmus OF8. J Bacteriol 176:1742–1749
    [Google Scholar]
  49. Sun J., Kahlow M. A., Kaysser T. M., Osbourne J. P., Hill J. J., Rohlfs R. J., Hille R., Gennis R. B., Loehr T. M. 1996; Resonance Raman spectroscopic identification of a histidine ligand of b 595 and the nature of the ligation of chlorin d in the fully reduced Escherichia coli cytochrome bd oxidase. Biochemistry 35:2403–2412
    [Google Scholar]
  50. Thorneley R. N. F., Ashby G. A. 1989; Oxidation of nitrogenase iron protein by dioxygen without inactivation could contribute to high respiratory rates of Aztobacter species and facilitate nitrogen fixation in other aerobic environments. Biochem J 261:181–187
    [Google Scholar]
  51. Tseng C.-P., Albrecht J., Gunsallus R. P. 1996; Effect of microaerophilic cell growth conditions on the expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHIJ, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli. . J Bacteriol 178:1094–1098
    [Google Scholar]
  52. Young J. P. W. 1992; Phylogenetic classification of nitrogen-fixing organisms. . In Biological Nitrogen Fixation pp. 43–86 . Edited by Stacey G., Burris R. H., Evans H. J. New York & London: Chapman & Hall;
    [Google Scholar]
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