1887

Microbiology Society logo

Volume 152, Issue 3

Evidence for a cytochrome interaction in the respiratory chain of Free

Abstract

Spectroscopic analysis of membranes isolated from , along with analysis of its genome, indicates that the cytochrome branch of its respiratory pathway consists of a modified complex that contains two cytochromes in its subunit, similar to other acid-fast bacteria, and an -type cytochrome oxidase. A functional association of the cytochrome and complexes was indicated by the findings that levels of detergent sufficient to completely disrupt isolated membranes failed to inhibit quinol-driven O reduction, but known inhibitors of the complex did inhibit quinol-driven O reduction. The gene for subunit II of the -type oxidase indicates the presence of additional charged residues in a predicted extramembrane domain, which could mediate an intercomplex association. However, high concentrations of monovalent salts had no effect on O reduction, suggesting that ionic interactions between extramembrane domains do not play the major role in stabilizing the interaction. Divalent cations did inhibit electron transfer, likely by distorting the electron-transfer interface between cytochrome and subunit II. Soluble cytochrome cannot donate electrons to the -type oxidase, even though key cytochrome -binding residues are conserved, probably because the additional residues of subunit II prevent the binding of soluble cytochrome . The results indicate that hydrophobic interactions are the primary forces maintaining the interaction, but ionic interactions may assist in aligning the two complexes for efficient electron transfer.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): DM, dodecyl β-d-maltoside , DMNQ, dimethylnaphthoquinone , DMNQH2, dimethylnaphthoquinol and TMPD, N,N,N′,N′-tetramethyl-p-phenylenediamine
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28723-0
2006-03-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/3/823.html?itemId=/content/journal/micro/10.1099/mic.0.28723-0&mimeType=html&fmt=ahah

References

  1. Assempour M, Lim D, Hill B. C. 1998; Electron transfer kinetics during the reduction and turnover of the cytochrome caa [sub]3[/sub] complex from Bacillus subtilus . Biochemistry 37:9991–9998 [CrossRef]
     [Google Scholar]
  2. Beggs M. L, Crawford J. T, Eisenach K. D. 1995; Isolation and sequencing of the replication region of Mycobacterium avium plasmid pLR7. J Bacteriol 177:4836–4840
     [Google Scholar]
  3. Bengtsson J, Tjalsma H, Rivolta C, Hederstedt L. 1999; Subunit II of Bacillus subtilis cytochrome c oxidase is a lipoprotein. J Bacteriol 181:685–688
     [Google Scholar]
  4. Bertsova Y. V, Bogachev A. V, Skulachev V. P. 1997; Generation of protonic potential by the bd -type quinol oxidase of Azotobacter vinelandii . FEBS Lett 414:369–372 [CrossRef]
     [Google Scholar]
  5. Castresana J, Lubben M, Saraste M, Heggins D. G. 1994; Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J 13:2516–2525
     [Google Scholar]
  6. Cole S. T, Brosch R, Parkhill J. & 39 other authors; 1998; Decifering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544 [CrossRef]
     [Google Scholar]
  7. Crinson M, Nicholls P. 1992; Routes of electron transfer in beef heart cytochrome c oxidase: is there a unique pathway used by all reductants?. Biochem Cell Biol 70:301–308 [CrossRef]
     [Google Scholar]
  8. Daldal F, Mandaci S, Winterstein C, Myllykallio H, Cuyck K, Zannoni D. 2001; Mobile cytochrome c [sub]2[/sub] and membrane-anchored cytochrome c [sub]y[/sub] are both efficient electron donors to the cbb [sub]3[/sub]- and aa [sub]3[/sub]-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides . J Biol Chem 183:2013–2024
     [Google Scholar]
  9. De Bruijn F. J, Rossbach S. 1994; Transposon mutagenesis. In Methods for General and Molecular Bacteriology pp  387–405 Edited by Gerhardt P. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  10. D'Mello R, Hill S, Poole R. K. 1996; The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142:755–763 [CrossRef]
     [Google Scholar]
  11. Drachev L. A, Jasaitis A. A, Kaulen A. D, Kondrashin A. A, Chu L. V, Semenov A. Y, Severina I. I, Skulachev V. P. 1976; Reconstitution of biological molecular generators of electric current. Cytochrome oxidase. J Biol Chem 251:7072–7076
     [Google Scholar]
  12. Gao X, Wen X, Esser L, Quinn B, Yu L, Yu C. A, Xia D. 2003; Structural basis for the quinone reduction in the bc [sub]1[/sub] complex: a comparative analysis of crystal structures of mitochondrial cytochrome bc [sub]1[/sub] with bound substrate and inhibitors at the Qi site. Biochemistry 42:9067–9080 [CrossRef]
     [Google Scholar]
  13. Hiser L, Valentin M. D, Hamer A. G, Hosler J. P. 2000; Cox11p is required for stable formation of the Cu[sub]B[/sub] and magnesium centers of cytochrome c oxidase. J Biol Chem 275:619–623 [CrossRef]
     [Google Scholar]
  14. Hosler J. P, Fetter J, Tecklenburg M. M. J, Espe M, Lerma C, Ferguson-Miller S. 1992; Cytochrome aa [sub]3[/sub] of Rhodobacter sphaeroides as a model for mitochondrial cytochrome c oxidase: purification, kinetics, proton pumping and spectral analysis. J Biol Chem 267:24264–24272
     [Google Scholar]
  15. Hosler J. P, Shapleigh J. P. 2002; Principles of aerobic respiration. In Encyclopedia of Environmental Microbiology pp  149–160 Edited by Bitton G. New York: Wiley;
     [Google Scholar]
  16. Junemann S. 1997; Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321107–127 [CrossRef]
     [Google Scholar]
  17. Jurtshuk P, Mueller T. J, Wong T. Y Jr. 1981; Isolation and purification of the cytochrome oxidase of Azotobacter vinelandii . Biochim Biophys Acta 637:374–382 [CrossRef]
     [Google Scholar]
  18. Kana B. D, Weinstein E. A, Avarbock D, Dawes S. S, Rubin H, Mizrahi V. 2001; Characterization of the cydAB -encoded cytochrome bd oxidase from Mycobacterium smegmatis . J Bacteriol 183:7076–7086 [CrossRef]
     [Google Scholar]
  19. 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]
  20. Lee B.-Y, Hefta S. A, Brennan P. J. 1992; Characterization of the major membrane protein of virulent Mycobacterium tuberculosis . Infect Immun 60:2066–2074
     [Google Scholar]
  21. Maneg O, Malatesta F, Ludwig B, Drosou V. 2004; Interaction of cytochrome c with cytochrome oxidase: two different docking scenarios. Biochim Biophys Acta 1655274–281 [CrossRef]
     [Google Scholar]
  22. Matsoso L. G, Kana B. V, Crellin P. K. 7 other authors 2005; Function of the cytochrome bc [sub]1[/sub]- aa [sub]3[/sub] branch of the respiratory network in mycobactera and network adaptation occurring in response to its disruption. J Bacteriol 187:6300–6308 [CrossRef]
     [Google Scholar]
  23. Niebisch A, Bott M. 2001; Molecular analysis of the cytochrome bc [sub]1[/sub]- aa [sub]3[/sub] branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c [sub]1[/sub]. Arch Microbiol 175:282–294 [CrossRef]
     [Google Scholar]
  24. Niebisch A, Bott M. 2003; Purification of a cytochrome bc-aa [sub]3[/sub] supercomplex with quinol oxidase activity from Corynebacterium glutamicum . Identification of a fourth subunit of cytochrome aa [sub]3[/sub] oxidase and mutational analysis of diheme cytochrome c [sub]1[/sub]. J Biol Chem 278:4339–4346 [CrossRef]
     [Google Scholar]
  25. Sakamoto J, Shibata T, Mine T, Miyahara R, Torigoe T, Noguchi S, Matsushita K, Sone N. 2001; Cytochrome c oxidase contains an extra charged amino acid cluster in a new type of respiratory chain in the amino-acid-producing Gram-positive bacterium Corynebacterium glutamicum . Microbiology 147:2865–2871
     [Google Scholar]
  26. 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]
  27. Sone N. 1990; Respiration-driven proton pumps. In The Bacteria pp  1–32 Edited by Krulwich T. A. New York: Academic Press;
     [Google Scholar]
  28. 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 1503279–290 [CrossRef]
     [Google Scholar]
  29. Sone N, Fukuda M, Katayama S, Jyoudai A, Syugyou M, Noguchi S, Sakamoto J. 2003; qcrCAB operon of a nocardia-form actinomycete Rhodococcus rhodochrous encodes cytochrome reductases complex with diheme cytochrome cc subunit. Biochim Biophys Acta 1557125–131 [CrossRef]
     [Google Scholar]
  30. Thony-Meyer L. 1997; Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61:337–376
     [Google Scholar]
  31. Wang K, Zhen Y, Sadoski R, Grinnell S, Geren L, Ferguson-Miller S, Durham B, Millett F. 1999; Definition of the interaction domain for cytochrome c on cytochrome c oxidase. II. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants. J Biol Chem 274:38042–38050 [CrossRef]
     [Google Scholar]
  32. Weinstein E. A, Yano T, Li L.-S. & 7 other authors; 2005; Inhibitors of type II NADH : menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci U S A 102:4548–4553 [CrossRef]
     [Google Scholar]
  33. Witt H, Malatesta F, Nicoletti F, Brunori M, Ludwig B. 1998; Cytochrome c binding site on cytochrome oxidase in Paracoccus denitrificans . Eur J Biochem 251:367–373 [CrossRef]
     [Google Scholar]
  34. Zhen Y, Hoganson C. W, Babcock G. T, Ferguson-Miller S. 1999; Definition of the interaction domain for cytochrome c on cytochrome c oxidase. I. Biochemical, spectral, and kinetic characterization of surface mutants in subunit II of Rhodobacter sphaeroides cytochrome aa [sub]3[/sub]. J Biol Chem 274:38032–38041 [CrossRef]
     [Google Scholar]
  35. Zhu W, Arceneaux J. E. L, Beggs M. L, Byers B. R, Eisenach K. D, Lundrigan M. D. 1998; Exochelin genes in Mycobacterium smegmatis : identification of an ABC transporter and two non-ribosomal peptide synthetase genes. Mol Microbiol 29:629–639 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28723-0
Loading
Evidence for a cytochrome bcc–aa3 interaction in the respiratory chain of Mycobacterium smegmatis
Microbiology 152, 823 (2006); https://doi.org/10.1099/mic.0.28723-0
/content/journal/micro/10.1099/mic.0.28723-0
/content/journal/micro/10.1099/mic.0.28723-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error