Relationship of Cytochrome caa3 from Thermus thermophilus to Other Heme- and Copper-Containing Terminal Oxidases

  • M. W. Mather
  • P. Springer
  • J. A. Fee
Part of the 41. Colloquium der Gesellschaft für Biologische Chemie 5.–7. April 1990 in Mosbach/Baden book series (MOSBACH, volume 41)


Cytochrome oxidases are a key component of the energy metabolism of most aerobic organisms from mammals to bacteria. They are the final enzyme of the membrane-associated respiratory chain responsible for converting the chemical energy of reduced substrates to a transmembrane electrochemical potential, which is used by the cell for a wide variety of energy-requiring processes. The most widely studied oxidase is the cytochrome c oxidase (cytochrome aa3 oxidase) of the mammalian mitochondrion. This complex, integral membrane protein contains 13 subunits and 4 canonical metal centers : heme centers, a and a3 ; copper centers, CuA and CuB. It is responsible for electron transfer from reduced cytochrome c to dioxygen with the concomitant reduction of dioxygen to water and the coupled vectorial transfer of protons across the mitochondrial membrane (see Chan and Li 1990; Palmer 1987 for recent reviews).


Oxidase Subunit Hydrophobic Segment Paracoccus Denitrificans Thermus Thermophilus Quinol Oxidase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson, S., de Bruijn, Coulson, A.R., Eperon, I.C., Sanger, F. & Young, I.G. (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J. Mol. Biol. 156:683–717PubMedCrossRefGoogle Scholar
  2. Annemtiller, S. & Schäfer, G. (1989) Cytochrome aa3 from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. FEBS Lett. 244:451–455CrossRefGoogle Scholar
  3. Anraku, Y. (1988) Bacterial electron transport chains. Annu. Rev. Biochem. 57:101–132PubMedCrossRefGoogle Scholar
  4. Bisson, R., Steffens, G.C.M. & Buse, G. (1982a) Localization of lipid binding domain(s) on subunit II of beef heart cytochrome c oxidase. J. Biol. Chem. 257:6716–6720PubMedGoogle Scholar
  5. Bisson, R., Steffens, G.C.M., Capaldi, R.A. & Buse, G. (1982b) Mapping of the cytochrome c binding site on cytochrome c oxidase. FEBS Lett. 144:359–363PubMedCrossRefGoogle Scholar
  6. Bonitz, S.G., Coruzzi, G., Thalenfeld, B.E. & Tzagoloff, A. (1980) Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit I of yeast cytochrome oxidase. J. Biol. Chem. 24:11927–11941Google Scholar
  7. Chan, S.I. & Li, P.M. (1990) Cytochrome c oxidase: understanding nature’s design of a proton pump. Biochemistry 29:1–12PubMedCrossRefGoogle Scholar
  8. Chepuri, V., Lemieux, L., Au, D.C.T. & Gennis, R.B. (1990) The Sequence of the cyo Operon Indicates Substantial Structural Similarities between the Cytochrome o Ubiquinol Oxidase of Escherichia coli and the aa 3-type Family of Cytochrome c Oxidases. J. Biol. Chem. 265:11185–11192PubMedGoogle Scholar
  9. Clary, D.O. & Wolstenholme, D.R. (1983a) Nucleotide sequence of a segment of Drosophila mitochondrial DNA that contains the genes for cytochrome c oxidase subunits II and III and ATPase subunit 6. Nucleic Acids Res. 11:4211–4227PubMedCrossRefGoogle Scholar
  10. Clary, D.O. & Wolstenholme, D.R. (1983b) Genes for cytochrome c oxidase subunit I, urf2, and 3 tRNA’s in Drosophila mitochondrial DNA. Nucleic Acids Res. 11:6859–6872PubMedCrossRefGoogle Scholar
  11. Coruzzi, G. & Tzagoloff, A. (1979) Assembly of mitochondrial membrane systems. DNA sequence of subunit 2 of yeast cytochrome oxidase. J. Biol. Chem. 254:9324–9330PubMedGoogle Scholar
  12. Dayhoff, M.O., Schwartz, R.M. & Orcutt, B.C. (1978) A model of evolutionary change in proteins. In: Dayhoff, M.O. (ed) Atlas of protein sequence and structure, vol. 5, suppl. 3. National Biomedical Research Foundation, Washington, D.C., pp. 345–352Google Scholar
  13. Degli Esposti, M., Ghelli, A., Luchetti, R., Crimi, M. & Lenaz, G. (1989) New approaches to the prediction of the folding of membrane proteins with redox function. Ital. J. Biochem. 38:1–22PubMedGoogle Scholar
  14. Devereux, J., Haeberli, P. & Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395PubMedCrossRefGoogle Scholar
  15. Doolittle, R.F. (1981) Similar amino acid sequences: chance or common ancestry? Science 214:149–159PubMedCrossRefGoogle Scholar
  16. Doolittle, R.F. (1986) Of urfs and orfs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, CaliforniaGoogle Scholar
  17. Einarsdöttir, O., Killough, P.M., Fee, J.A. & Woodruff, W.H. (1989) An infrared study of the binding and photodissociation of carbon monoxide in cytochrome ba3 from Thermus thermophilus. J. Biol. Chem. 264:2405–2408PubMedGoogle Scholar
  18. Fee, J.A., Kuila, D., Mather, M.W. & Yoshida, T. (1986) Respiratory proteins from extremely thermophilic, aerobic bacteria. Biochim. Biophys. Acta 853:153–185PubMedGoogle Scholar
  19. Fee, J.A., Mather, M.W., Springer, P., Hensel, S. & Buse, G. (1988) Isolation and partial sequence of the A-protein gene of Thermus thermophilus cytochrome q aa3. Ann. New York Acad. Sci. 550:33–38CrossRefGoogle Scholar
  20. Gelles, J., Blair, D.F. & Chan, S.I. (1986) The proton-pumping site of cytochrome c oxidase: a model of its structure and mechanism. Biochim. Biophys. Acta 853:205–236PubMedGoogle Scholar
  21. Gribskov, M., McLachlan, A.D. & Eisenberg, D. (1987) Profile analysis: detection of distantly related proteins. Proc. Natl. Acad. Sci. USA 84:4355–4358PubMedCrossRefGoogle Scholar
  22. Hata, A., Kirino, Y., Matsuura, K., Itoh, S., Hiyama, T., Konishi, K., Kita, K. & Anraku, Y. (1985) Assignment of ESR signals of Escherichia coli terminal oxidase complexes. Biochim. Biophys. Acta 810:62–72PubMedCrossRefGoogle Scholar
  23. Holm, L., Saraste, M. & Wikström, M. (1987) Structural models of the redox centres in cytochrome oxidase. EMBO J. 6:2819–2823PubMedGoogle Scholar
  24. Hon-nami, K. & Oshima, T. (1984) Purification and characterization of cytochrome c oxidase from Thermus thermophilus HB8. Biochemistry 23:454–460CrossRefGoogle Scholar
  25. Ishizuka, M., Machida, K., Shimada, I. & Sone, N. (1990) (submitted)Google Scholar
  26. Kita, K., Konishi, K. & Anraku, Y. (1984) Terminal oxidases of Escherichia coli aerobic respiratory chain. J. Biol. Chem. 259:3368–3374PubMedGoogle Scholar
  27. Kyte, J. & Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105–132PubMedCrossRefGoogle Scholar
  28. Martin, C.T., Scholes, C.P. & Chan, S.I. (1988) On the nature of cysteine coordination to CuA in cytochrome c oxidase. J. Biol. Chem 263:8420–8429PubMedGoogle Scholar
  29. Mather, M.W. (1988) Base composition-independent hybridization in dried agarose gels: screening and recovery for cloning of genomic DNA fragments. Bio Techniques 6:444–447Google Scholar
  30. Mather, M.W., Springer, P., & Fee, J.A. (1990) (submitted)Google Scholar
  31. Michel, H., Weyer, K.A., Gruenberg, H., Dünger, I., Oesterhelt, D. & Lottspeich, F. (1986) The ‘light’ and ‘medium’ subunits of the photosynthetic reaction centre from Rhodospeudomonas viridis: isolation of the genes, nucleotide and amino acid sequence. EMBO J. 5:1149–1158PubMedGoogle Scholar
  32. Millet, F., de Jong, C., Paulson, L. & Capaldi, R.A. (1983) Identification of specific carboxylate groups on cytochrome c oxidase that are involved in binding cytochrome c. Biochemistry 22:546–552CrossRefGoogle Scholar
  33. Müller, M., Schläpfer, B. & Azzi, A. (1988a) Preparation of a one-subunit cytochrome oxidase from Paracoccus denitrificans: spectral analysis and enzymatic activity. Biochemistry 27:7546–7551PubMedCrossRefGoogle Scholar
  34. Müller, M., SchJäpfer, B. & Azzi, A. (1988b) Cytochrome c oxidase from Paracoccus denitrificans: both hemes are located in subunit I. Proc. Natl. Acad. Sci. USA 85:6647–6651PubMedCrossRefGoogle Scholar
  35. Palmer, G. (1987) Cytochrome oxidase: a perspective. Pure Appl. Chem. 59:749–758CrossRefGoogle Scholar
  36. Puustinen, A., Finel, M., Virkki, M. & Wikström, M. (1989) Cytochrome o (bo) is a proton pump in Paracoccus denitrificans and Escherichia coli. FEBS Lett. 249:163–167PubMedCrossRefGoogle Scholar
  37. Raitio, M., Tuulikki, J. & Saraste, M. (1987) Isolation and analysis of the genes for cytochrome c oxidase in Paracoccus denitrificans. EMBO J. 6:2825–2833PubMedGoogle Scholar
  38. Robillard, G.T. & Lolkema, J.S. (1988) Enzymes II of the phosphoeno/pyruvate-dependent sugar transport systems: a review of their structure and mechanism of sugar transport. Biochim. Biophys. Acta 947:493–519PubMedGoogle Scholar
  39. Salerno, J.C., Bolgiano, B. & Ingledew, W.J. (1989) Potentiometrie titration of cytochrome-bo type quinol oxidase of Escherichia coli: evidence for heme-heme and copper-heme interaction. FEBS Lett. 247:101–105PubMedCrossRefGoogle Scholar
  40. Sanger, F., Nicklen, S. & Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. USA 74:5463–5467CrossRefGoogle Scholar
  41. Saraste, M., Raitio, M., Tuulikki, J. & Perämaa, A. (1986) A gene in Paracoccus for subunit III of cytochrome oxidase. FEBS Lett. 206:154–156PubMedCrossRefGoogle Scholar
  42. Sone, N., Yanagita, Y., Hon-Nami, K., Fukumori, Y. & Yamanaka, T. (1983) Proton-pump activity of Nitrobacter agilis and Thermus thermophilus cytochrome c oxidases. FEBS Lett 155:150–154CrossRefGoogle Scholar
  43. Sone, N., Yokoi, F., Fu, T., Ohta, S., Metso, T., Raitio, M. & Saraste, M. (1988) Nucleotide sequence of the gene coding for cytochrome oxidase subunit I from the thermophilic bacterium PS3. J. Biochem. (Tokyo) 103:606–610Google Scholar
  44. Steffens, G.J. & Buse, G. (1979) Studies on cytochrome c oxidase, IV. Primary structure and function of subunit II. Hoppe-Seyler’s Z. Physiol. Chem. 360:613–619Google Scholar
  45. Steinrücke, P., Steffens, G.C.M., Panskus, G., Buse, G. & Ludwig, B. (1987) Subunit II of cytochrome c oxidase from Paracoccus denitrificans. DNA sequence, gene expression and the protein. Eur. J. Biochem. 167:431–439PubMedCrossRefGoogle Scholar
  46. Sweet, R.M. & Eisenberg, D. (1983) Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structures. J. Mol. Biol. 171:479–488PubMedCrossRefGoogle Scholar
  47. Thalenfeld, B.E. & Tzagoloff, A. (1980) Assembly of the mitochondrial membrane system. Sequence of the Oxi2 gene of yeast mitochondrial DNA. J. Biol. Chem. 255:6173–6180PubMedGoogle Scholar
  48. Wikström, M., Saraste, M. & Pentillä, T. (1985) Relationships between structure and function in cytochrome oxidase. In: Martonosi, A.M. (ed) The enzymes of biological membranes, vol. 4. Plenum, New YorkGoogle Scholar
  49. Woese, C.R. (1987) Bacterial evolution. Microbiol. Rev. 51:221–271PubMedGoogle Scholar
  50. Yoshida, T. & Fee, J.A. (1984) Studies on cytochrome c oxidase activity of the cytochrome c1aa3 complex from Thermus thermophilus. J. Biol. Chem. 529:1031–1036Google Scholar
  51. Yoshida, T., Lorence, R.M., Choc, M.G., Tarr, G.E., Findling, K.L. & Fee, J.A. (1984) Respiratory proteins from the extremely thermophilic aerobic bacterium, Thermus thermophilus. J. Biol. Chem. 259:112–123PubMedGoogle Scholar
  52. Zimmermann, B.H., Nitsche, C.I., Fee, J.A., Rusnak, F. & Münck, E. (1988) Properties of a copper-containing cytochrome ba3: a second terminal oxidase from the extreme thermophile Thermus thermophilus. Proc. Natl. Acad. Sci. USA 85:5779–5783PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • M. W. Mather
  • P. Springer
  • J. A. Fee
    • 1
  1. 1.Biochemistry Section and Stable Isotope ResourceIsotope and Structural Chemistry Group, Los Alamos National LaboratoryLos AlamosUSA

Personalised recommendations