1887

Abstract

The membranes from cells contain a hydrophobic di-haem C protein as the cytochrome subunit of the new type of cytochrome complex (complex III in the respiratory chain) encoded by the operon [Sone, N., Nagata, K., Kojima, H., Tajima, J., Kodera, Y., Kanamaru, T., Noguchi, S. & Sakamoto, J. (2001). 1503, 279–290]. To characterize complex IV, cytochrome oxidase and its structural genes were isolated. The oxidase is of the cytochrome type, but mass spectrometry indicated that the haem is haem As, which contains a geranylgeranyl side-chain instead of a farnesyl group. The enzyme is a SoxM-type haem–copper oxidase composed of three subunits. Edman degradation and mass spectrometry suggested that the N-terminal signal sequence of subunit II is cleaved and that the new N-terminal cysteine residue is diacylglycerated, while neither subunit I nor subunit III is significantly modified. The genes for subunits II () and III () are located upstream of the operon, while that for subunit I () is located separately. The oxidase showed low enzyme activity with extrinsic substrates such as cytochromes from horse heart or yeast, and has the Cu-binding motif in its subunit II. A prominent structural feature is the insertion of an extra charged amino acid cluster between the β2 and β4 strands in the substrate-binding domain of subunit II. The β2–β4 loop of this oxidase is about 30 residues longer than that of major cytochrome oxidases from mitochondria and proteobacteria, and is rich in both acidic and basic residues. These findings suggest that the extra charged cluster may play a role in the interaction of the oxidase with the cytochrome subunit of the new type of complex.

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2001-10-01
2019-12-16
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References

  1. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puustinen, A., Iwata, S. & Wikström, M. ( 2000; ). The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat Struct Biol 7, 910-917.[CrossRef]
    [Google Scholar]
  2. Bengtsson, J., Thalsma, H., Rivolta, C. & Hederstedt, L. ( 1999; ). Subunit II of Bacillus subtilis cytochrome c oxidase is a lipoprotein. J Bacteriol 181, 685-688.
    [Google Scholar]
  3. Castresana, J. & Saraste, M. ( 1995; ). Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem Sci 20, 443-448.[CrossRef]
    [Google Scholar]
  4. Cole, S. T., Brosch, R., Parkhill, J. & 39 other authors ( 1998; ). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537–544.[CrossRef]
    [Google Scholar]
  5. Ghaim, J. B., Tsatsos, P. H., Katsonouri, A., Mitchell, D. M., Salcedo-Hernandez, R. & Gennis, R. B. ( 1997; ). Matrix-assisted laser desorption ionization mass spectrometry of membrane proteins: demonstration of a simple method to determine subunit molecular weights of hydrophobic subunits. Biochim Biophys Acta 1330, 113-120.[CrossRef]
    [Google Scholar]
  6. Ishizuka, M., Machida, K., Shimada, S., Mogi, A., Tsuchiya, T., Ohmori, T., Souma, Y., Gonda, M. & Sone, N. ( 1990; ). Nucleotide sequences of the genes coding for four subunits of cytochrome c oxidase from the thermophilic bacterium, PS3. J Biochem 108, 866-873.
    [Google Scholar]
  7. Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. ( 1995; ). Structure at 2·8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669.[CrossRef]
    [Google Scholar]
  8. Kusumoto, K., Sakiyama, M., Sakamoto, J., Noguchi, S. & Sone, N. ( 2000; ). Menaquinol oxidase activity and primary structure of cytochrome bd from the amino-acid fermenting bacterium Corynebacterium glutamicum. Arch Microbiol 173, 390-397.[CrossRef]
    [Google Scholar]
  9. Lübben, M. & Morand, K. ( 1994; ). Novel prenylated hemes as cofactors of cytochrome oxidases. Archaea have modified hemes A and O. J Biol Chem 269, 21473-21479.
    [Google Scholar]
  10. Ma, J., Katsonouri, A. & Gennis, R. B. ( 1997; ). Subunit II of the cytochrome bo 3 ubiquinol oxidase from Escherichia coli is a lipoprotein. Biochemistry 36, 11298-11303.[CrossRef]
    [Google Scholar]
  11. Noguchi, S., Yamazaki, T., Yaginuma, A., Sakamoto, J. & Sone, N. ( 1994; ). Overexpression of membrane-bound cytochrome c-551 from thermophilic Bacillus PS3 in Bacillus stearothermophilus K1041. Biochim Biophys Acta 1188, 302-310.[CrossRef]
    [Google Scholar]
  12. Quirk, P. G., Hicks, D. B. & Krulwich, T. A. ( 1993; ). Cloning of the cta operon from alkaliphilic Bacillus firmus OF4 and characterization of the pH-regulated cytochrome caa 3 oxidase it encodes. J Biol Chem 268, 678-685.
    [Google Scholar]
  13. Sakamoto, J., Matsumoto, A., Oobuchi, K. & Sone, N. ( 1996; ). Cytochrome bd-type quinol oxidase in a mutant of Bacillus stearothermophilus deficient in caa 3-type cytochrome c oxidase. FEMS Microbiol Lett 143, 151-158.[CrossRef]
    [Google Scholar]
  14. Sakamoto, J., Handa, Y. & Sone, N. ( 1997; ). A novel cytochrome b(o/a) 3-type oxidase from Bacillus stearothermophilus catalyzes cytochrome c-551 oxidation. J Biochem 122, 764-771.[CrossRef]
    [Google Scholar]
  15. Sakamoto, J., Koga, E., Mizuta, T., Sato, C., Noguchi, S. & Sone, N. ( 1999; ). Gene structure and quinol oxidase activity of a cytochrome bd-type oxidase from Bacillus stearothermophilus. Biochim Biophys Acta 1411, 147-158.[CrossRef]
    [Google Scholar]
  16. Sone, N. & Yanagita, Y. ( 1982; ). A cytochrome aa 3-type terminal oxidase of a thermophilic bacterium: purification, properties and proton pumping. Biochim Biophys Acta 682, 216-226.[CrossRef]
    [Google Scholar]
  17. Sone, N., Sekimachi, M. & Kutoh, E. ( 1987; ). Identification and properties of a quinol oxidase super-complex composed of a bc 1 complex and cytochrome oxidase in the thermophilic bacterium, PS3. J Biol Chem 262, 15386-15391.
    [Google Scholar]
  18. Sone, N., Nagata, K., Kojima, H., Tajima, J., Kodera, Y., Kanamaru, T., Noguchi, S. & Sakamoto, J. ( 2001; ). A novel hydrophobic diheme c-type cytochrome. Purification from Corynebacterium glutamicum and analysis of the QcrCBA operon encoding three subunit proteins of a putative cytochrome reductase complex. Biochim Biophys Acta 1503, 279-290.[CrossRef]
    [Google Scholar]
  19. Soulimane, T., Buse, G., Bourenkov, G. P., Bartunik, H. D., Huber, R. & Than, M. E. ( 2000; ). Structure and mechanism of the aberrant ba 3-cytochrome c oxidase from Thermus thermophilus. EMBO J 19, 1766-1776.[CrossRef]
    [Google Scholar]
  20. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.[CrossRef]
    [Google Scholar]
  21. Tomb, J.-F., White, O., Kerlavage, A. R. & 39 other authors ( 1997; ). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547.[CrossRef]
    [Google Scholar]
  22. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R. & Yoshikawa, S. ( 1996; ). The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2·8 Å. Science 272, 1136-114.[CrossRef]
    [Google Scholar]
  23. von Wachenfeldt, C. & Hederstedt, L. ( 1993; ). Physico-chemical characterisation of membrane-bound and water-soluble forms of Bacillus subtilis cytochrome c-550. Eur J Biochem 212, 499-509.[CrossRef]
    [Google Scholar]
  24. Xiong, J., Inoue, K. & Bauer, C. E. ( 1998; ). Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95, 14851-14856.[CrossRef]
    [Google Scholar]
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