Advertisement

Integral caa3-Cytochrome c Oxidase from Thermus thermophilus: Purification and Crystallization

  • Orla SlatteryEmail author
  • Sabri Cherrak
  • Tewfik Soulimane
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2039)

Abstract

Cytochrome c oxidase is a respiratory enzyme catalyzing the energy-conserving reduction of molecular oxygen to water—a fundamental biological process of cell respiration. The first crystal structures of the type A cytochrome c oxidases, bovine heart and Paracoccus denitrificans cytochrome c oxidases, were published in 1995 and contributed immensely to the understanding of the enzyme’s mechanism of action. The senior author’s research focus was directed toward understanding the structure and function of the type B cytochrome c oxidases, ba3-oxidase and type A2 caa3-oxidase, both from the extreme thermophilic bacterium Thermus thermophilus. While the ba3-oxidase structure was published in 2000 and functional characterization is well-documented in the literature, we recently successfully solved the structure of the caa3-nature made enzyme-substrate complex. This chapter is dedicated to the purification and crystallization process of caa3-cytochrome c oxidase.

Key words

Cytochrome c oxidase caa3-Oxidase Chromatography Crystallization Bioenergetics Thermus thermophilus 

References

  1. 1.
    Ferguson-Miller S, Babcock GT (1996) Heme/copper terminal oxidases. Chem Rev 96:2889–2908CrossRefGoogle Scholar
  2. 2.
    Michel H, Behr J, Harrenga A, Kannt A (1998) Cytochrome C oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329–356.  https://doi.org/10.1146/annurev.biophys.27.1.329CrossRefPubMedGoogle Scholar
  3. 3.
    Tsukihara T, Aoyama H, Yamashita E et al (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272:1136–1144CrossRefGoogle Scholar
  4. 4.
    Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669.  https://doi.org/10.1038/376660a0CrossRefPubMedGoogle Scholar
  5. 5.
    Soulimane T, Buse G, Bourenkov GP et al (2000) Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from thermus thermophilus. EMBO J 19:1766–1776.  https://doi.org/10.1093/emboj/19.8.1766CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Svensson-Ek M, Abramson J, Larsson G et al (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J Mol Biol 321:329–339CrossRefGoogle Scholar
  7. 7.
    Buschmann S, Warkentin E, Xie H et al (2010) The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science 329:327–330.  https://doi.org/10.1126/science.1187303CrossRefPubMedGoogle Scholar
  8. 8.
    Lyons JA, Aragão D, Slattery O et al (2012) Structural insights into electron transfer in caa3-type cytochrome oxidase. Nature 487:514–518.  https://doi.org/10.1038/nature11182CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    OSHIMA T, IMAHORI K (1974) Description of Thermus thermophilus (Yoshida and Oshima) comb. nov., a nonsporulating thermophilic bacterium from a Japanese thermal spa. Int J Syst Bacteriol 24:102–112.  https://doi.org/10.1099/00207713-24-1-102CrossRefGoogle Scholar
  10. 10.
    Rich PR (2003) The molecular machinery of Keilin’s respiratory chain. Biochem Soc Trans 31:1095–1105CrossRefGoogle Scholar
  11. 11.
    Haltia T, Finel M, Harms N et al (1989) Deletion of the gene for subunit III leads to defective assembly of bacterial cytochrome oxidase. EMBO J 8:3571–3579CrossRefGoogle Scholar
  12. 12.
    Riistama S, Puustinen A, García-Horsman A et al (1996) Channelling of dioxygen into the respiratory enzyme. Biochim Biophys Acta 1275:1–4CrossRefGoogle Scholar
  13. 13.
    Fee JA, Choc MG, Findling KL et al (1980) Properties of a copper-containing cytochrome c1aa3 complex: a terminal oxidase of the extreme thermophile Thermus thermophilus HB8. Proc Natl Acad Sci U S A 77:147–151CrossRefGoogle Scholar
  14. 14.
    Mather MW, Springer P, Hensel S et al (1993) Cytochrome oxidase genes from Thermus thermophilus. Nucleotide sequence of the fused gene and analysis of the deduced primary structures for subunits I and III of cytochrome caa3. J Biol Chem 268:5395–5408PubMedGoogle Scholar
  15. 15.
    Mather MW, Springer P, Fee JA (1991) Cytochrome oxidase genes from Thermus thermophilus. Nucleotide sequence and analysis of the deduced primary structure of subunit IIc of cytochrome caa3. J Biol Chem 266:5025–5035PubMedGoogle Scholar
  16. 16.
    Than ME, Hof P, Huber R et al (1997) Thermus thermophilus cytochrome-c552: a new highly thermostable cytochrome-c structure obtained by MAD phasing. J Mol Biol 271:629–644.  https://doi.org/10.1006/jmbi.1997.1181CrossRefPubMedGoogle Scholar
  17. 17.
    Lecomte S, Hilleriteau C, Forgerit JP et al (2001) Structural changes of cytochrome c(552) from Thermus thermophilus adsorbed on anionic and hydrophobic surfaces probed by FTIR and 2D-FTIR spectroscopy. Chembiochem 2:180–189CrossRefGoogle Scholar
  18. 18.
    Janzon J, Ludwig B, Malatesta F (2007) Electron transfer kinetics of soluble fragments indicate a direct interaction between complex III and the caa3 oxidase in Thermus thermophilus. IUBMB Life 59:563–569.  https://doi.org/10.1080/15216540701242482CrossRefPubMedGoogle Scholar
  19. 19.
    Schrodinger L PyMOL Molecular Graphics System, Version 2.0. Schrödinger, LLC, New York, NYGoogle Scholar
  20. 20.
    Sousa PMF, Videira M a M, Bohn A et al (2012) The aerobic respiratory chain of Escherichia coli: from genes to supercomplexes. Microbiology 158:2408–2418.  https://doi.org/10.1099/mic.0.056531-0CrossRefPubMedGoogle Scholar
  21. 21.
    Brzezinski P (2004) Redox-driven membrane-bound proton pumps. Trends Biochem Sci 29:380–387.  https://doi.org/10.1016/j.tibs.2004.05.008CrossRefPubMedGoogle Scholar
  22. 22.
    Giuffrè A, Stubauer G, Sarti P et al (1999) The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications. Proc Natl Acad Sci U S A 96:14718–14723CrossRefGoogle Scholar
  23. 23.
    Castenholz RW (1969) Thermophilic blue-green algae and the thermal environment. Bacteriol Rev 33:476–504PubMedPubMedCentralGoogle Scholar
  24. 24.
    Keightley JA, Zimmermann BH, Mather MW et al (1995) Molecular genetic and protein chemical characterization of the cytochrome ba3 from Thermus thermophilus HB8. J Biol Chem 270:20345–20358 CrossRefGoogle Scholar
  25. 25.
    Cheng A, Hummel B, Qiu H, Caffrey M (1998) A simple mechanical mixer for small viscous lipid-containing samples. Chem Phys Lipids 95:11–21CrossRefGoogle Scholar
  26. 26.
    Caffrey M, Cherezov V (2009) Crystallizing membrane proteins using lipidic mesophases. Nat Protoc 4:706–731.  https://doi.org/10.1038/nprot.2009.31CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Cherezov V, Caffrey M, IUCr (2003) Nano-volume plates with excellent optical properties for fast, inexpensive crystallization screening of membrane proteins. J Appl Crystallogr 36:1372–1377.  https://doi.org/10.1107/S002188980301906XCrossRefGoogle Scholar
  28. 28.
    van Gelder BF (1966) On cytochrome c oxidase. I. The extinction coefficients of cytochrome a and cytochrome a3. Biochim Biophys Acta 118:36–46CrossRefGoogle Scholar
  29. 29.
    Mooser D, Maneg O, Corvey C et al (2005) A four-subunit cytochrome bc(1) complex complements the respiratory chain of Thermus thermophilus. Biochim Biophys Acta 1708:262–274.  https://doi.org/10.1016/j.bbabio.2005.03.008CrossRefPubMedGoogle Scholar
  30. 30.
    Mooser D, Maneg O, MacMillan F et al (2006) The menaquinol-oxidizing cytochrome bc complex from Thermus thermophilus: protein domains and subunits. Biochim Biophys Acta 1757:1084–1095.  https://doi.org/10.1016/j.bbabio.2006.05.033CrossRefPubMedGoogle Scholar
  31. 31.
    Soulimane T (1993) Activity and preparation for crystallisation of various cytochrome oxidase preparations. Rheinish-Westfalishen Technishen Hochshule, AachenGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Orla Slattery
    • 1
    • 2
    Email author
  • Sabri Cherrak
    • 1
    • 3
  • Tewfik Soulimane
    • 1
  1. 1.Department of Chemical Sciences, Bernal InstituteUniversity of LimerickLimerickIreland
  2. 2.Department of Biopharmaceutical and Medical ScienceGalway-Mayo Institute of TechnologyGalwayIreland
  3. 3.Department of BiologyUniversity Abou-Bekr BelkaidTlemcenAlgeria

Personalised recommendations