Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase

Izumi Ishigami, Ariel Lewis-Ballester, Austin Echelmeier, Gerrit Brehm, Nadia Zatsepin, Thomas D. Grant, Jesse D. Coe, Stella Lisova, Garrett Nelson, Shangji Zhang, Zachary F. Dobson, Sébastien Boutet, Raymond G. Sierra, Alexander Batyuk, Petra Fromme, Raimund Fromme, John Spence, Alexandra Ros, Syun Ru Yeh, Denis L. Rousseau

    Research output: Contribution to journalArticle

    1 Citation (Scopus)

    Abstract

    Cytochrome c oxidase (CcO) reduces dioxygen to water and harnesses the chemical energy to drive proton translocation across the inner mitochondrial membrane by an unresolved mechanism. By using time-resolved serial femtosecond crystallography, we identified a key oxygen intermediate of bovine CcO. It is assigned to the P R -intermediate, which is characterized by specific redox states of the metal centers and a distinct protein conformation. The heme a 3 iron atom is in a ferryl (Fe 4+ = O 2− ) configuration, and heme a and Cu B are oxidized while Cu A is reduced. A Helix-X segment is poised in an open conformational state; the heme a farnesyl sidechain is H-bonded to S382, and loop-I-II adopts a distinct structure. These data offer insights into the mechanism by which the oxygen chemistry is coupled to unidirectional proton translocation.

    Original languageEnglish (US)
    Pages (from-to)3572-3577
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume116
    Issue number9
    DOIs
    StatePublished - Feb 26 2019

    Fingerprint

    Electron Transport Complex IV
    Oxygen
    Protons
    Protein Conformation
    Crystallography
    Mitochondrial Membranes
    Oxidation-Reduction
    Iron
    Metals
    Water
    heme a

    Keywords

    • Bioenergetics
    • Catalytic intermediates
    • Complex IV
    • Crystallography
    • X-ray free electron laser

    ASJC Scopus subject areas

    • General

    Cite this

    Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. / Ishigami, Izumi; Lewis-Ballester, Ariel; Echelmeier, Austin; Brehm, Gerrit; Zatsepin, Nadia; Grant, Thomas D.; Coe, Jesse D.; Lisova, Stella; Nelson, Garrett; Zhang, Shangji; Dobson, Zachary F.; Boutet, Sébastien; Sierra, Raymond G.; Batyuk, Alexander; Fromme, Petra; Fromme, Raimund; Spence, John; Ros, Alexandra; Yeh, Syun Ru; Rousseau, Denis L.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 9, 26.02.2019, p. 3572-3577.

    Research output: Contribution to journalArticle

    Ishigami, I, Lewis-Ballester, A, Echelmeier, A, Brehm, G, Zatsepin, N, Grant, TD, Coe, JD, Lisova, S, Nelson, G, Zhang, S, Dobson, ZF, Boutet, S, Sierra, RG, Batyuk, A, Fromme, P, Fromme, R, Spence, J, Ros, A, Yeh, SR & Rousseau, DL 2019, 'Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase' Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 9, pp. 3572-3577. https://doi.org/10.1073/pnas.1814526116
    Ishigami, Izumi ; Lewis-Ballester, Ariel ; Echelmeier, Austin ; Brehm, Gerrit ; Zatsepin, Nadia ; Grant, Thomas D. ; Coe, Jesse D. ; Lisova, Stella ; Nelson, Garrett ; Zhang, Shangji ; Dobson, Zachary F. ; Boutet, Sébastien ; Sierra, Raymond G. ; Batyuk, Alexander ; Fromme, Petra ; Fromme, Raimund ; Spence, John ; Ros, Alexandra ; Yeh, Syun Ru ; Rousseau, Denis L. / Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 9. pp. 3572-3577.
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