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

Abstract

Cytochrome c oxidase (C c O) 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 C c O. 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.

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ; ; ORCiD logo;
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1494322
Alternate Identifier(s):
OSTI ID: 1506175
Grant/Contract Number:  
AC02-76SF00515; GM098799; GM126297; GM115773; GM095583; CHE-1404929; ABI-1565180; STC-1231306
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 9; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; bioenergetics; complex IV; X-ray free electron laser; crystallography; catalytic intermediates

Citation Formats

Ishigami, Izumi, Lewis-Ballester, Ariel, Echelmeier, Austin, Brehm, Gerrit, Zatsepin, Nadia A., 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 C. H., Ros, Alexandra, Yeh, Syun-Ru, and Rousseau, Denis L. Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. United States: N. p., 2019. Web. https://doi.org/10.1073/pnas.1814526116.
Ishigami, Izumi, Lewis-Ballester, Ariel, Echelmeier, Austin, Brehm, Gerrit, Zatsepin, Nadia A., 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 C. H., Ros, Alexandra, Yeh, Syun-Ru, & Rousseau, Denis L. Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. United States. https://doi.org/10.1073/pnas.1814526116
Ishigami, Izumi, Lewis-Ballester, Ariel, Echelmeier, Austin, Brehm, Gerrit, Zatsepin, Nadia A., 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 C. H., Ros, Alexandra, Yeh, Syun-Ru, and Rousseau, Denis L. Mon . "Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase". United States. https://doi.org/10.1073/pnas.1814526116.
@article{osti_1494322,
title = {Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase},
author = {Ishigami, Izumi and Lewis-Ballester, Ariel and Echelmeier, Austin and Brehm, Gerrit and Zatsepin, Nadia A. and Grant, Thomas D. and Coe, Jesse D. and Lisova, Stella and Nelson, Garrett and Zhang, Shangji and Dobson, Zachary F. and Boutet, Sébastien and Sierra, Raymond G. and Batyuk, Alexander and Fromme, Petra and Fromme, Raimund and Spence, John C. H. and Ros, Alexandra and Yeh, Syun-Ru and Rousseau, Denis L.},
abstractNote = {Cytochrome c oxidase (C c O) 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 C c O. 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.},
doi = {10.1073/pnas.1814526116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 9,
volume = 116,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1814526116

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Cited by: 12 works
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