skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 [1];  [1];  [2];  [3];  [2];  [4];  [2];  [2];  [2];  [2];  [2];  [5];  [5]; ORCiD logo [5];  [2];  [2];  [2];  [2]; ORCiD logo [1];  [1]
  1. Albert Einstein College of Medicine, Bronx, NY (United States)
  2. Arizona State Univ., Tempe, AZ (United States)
  3. Arizona State Univ., Tempe, AZ (United States); Univ. of Goettingen, Goettingen (Germany)
  4. Hauptman-Woodward Institute and SUNY Univ. of Buffalo, Buffalo, NY (United States)
  5. SLAC National Accelerator Lab., Menlo Park, CA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1494322
Alternate Identifier(s):
OSTI ID: 1506175
Grant/Contract Number:  
GM098799; GM126297; GM115773; GM095583; AC02-76SF00515; 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 Volume: 116; Journal Issue: 9; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
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. doi: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. doi: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. doi: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
DOI: 10.1073/pnas.1814526116

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Polder maps: improving OMIT maps by excluding bulk solvent
journal, February 2017

  • Liebschner, Dorothee; Afonine, Pavel V.; Moriarty, Nigel W.
  • Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 2, p. 148-157
  • DOI: 10.1107/S2059798316018210

Femtosecond X-ray protein nanocrystallography
journal, February 2011

  • Chapman, Henry N.; Fromme, Petra; Barty, Anton
  • Nature, Vol. 470, Issue 7332, p. 73-77
  • DOI: 10.1038/nature09750