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

Izumi Ishigami; Ariel Lewis-Ballester; Austin Echelmeier; Gerrit Brehm; Nadia A. 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 C.H. Spence; Alexandra Ros; Syun Ru Yeh; Denis L. Rousseau

doi:10.1073/pnas.1814526116

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

Izumi Ishigami
, Ariel Lewis-Ballester
, Austin Echelmeier
, Gerrit Brehm
, Nadia A. 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 C.H. Spence
, Alexandra Ros
, Syun Ru Yeh
, Denis L. Rousseau

Research output: Contribution to journal › Article › peer-review

87 Scopus citations

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 language	English (US)
Pages (from-to)	3572-3577
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	9
DOIs	https://doi.org/10.1073/pnas.1814526116
State	Published - Feb 26 2019

Keywords

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

ASJC Scopus subject areas

General

Access to Document

10.1073/pnas.1814526116

Cite this

Ishigami, I., Lewis-Ballester, A., Echelmeier, A., Brehm, G., Zatsepin, N. A., Grant, T. D., Coe, J. D., Lisova, S., Nelson, G., Zhang, S., Dobson, Z. F., Boutet, S., Sierra, R. G., Batyuk, A., Fromme, P., Fromme, R., Spence, J. C. H., Ros, A., Yeh, S. R., & Rousseau, D. L. (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, 116(9), 3572-3577. https://doi.org/10.1073/pnas.1814526116

Ishigami, I, Lewis-Ballester, A, Echelmeier, A, Brehm, G, Zatsepin, NA, Grant, TD, Coe, JD, Lisova, S, Nelson, G, Zhang, S, Dobson, ZF, Boutet, S, Sierra, RG, Batyuk, A, Fromme, P , Fromme, R, Spence, JCH, 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

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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.",

keywords = "Bioenergetics, Catalytic intermediates, Complex IV, Crystallography, X-ray free electron laser",

author = "Izumi Ishigami and Ariel Lewis-Ballester and Austin Echelmeier and Gerrit Brehm and Zatsepin, \{Nadia A.\} and Grant, \{Thomas D.\} and Coe, \{Jesse D.\} and Stella Lisova and Garrett Nelson and Shangji Zhang and Dobson, \{Zachary F.\} and S{\'e}bastien Boutet and Sierra, \{Raymond G.\} and Alexander Batyuk and Petra Fromme and Raimund Fromme and Spence, \{John C.H.\} and Alexandra Ros and Yeh, \{Syun Ru\} and Rousseau, \{Denis L.\}",

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AU - Ishigami, Izumi

AU - Lewis-Ballester, Ariel

AU - Echelmeier, Austin

AU - Brehm, Gerrit

AU - Zatsepin, Nadia A.

AU - Grant, Thomas D.

AU - Coe, Jesse D.

AU - Lisova, Stella

AU - Nelson, Garrett

AU - Zhang, Shangji

AU - Dobson, Zachary F.

AU - Boutet, Sébastien

AU - Sierra, Raymond G.

AU - Batyuk, Alexander

AU - Fromme, Petra

AU - Fromme, Raimund

AU - Spence, John C.H.

AU - Ros, Alexandra

AU - Yeh, Syun Ru

AU - Rousseau, Denis L.

PY - 2019/2/26

Y1 - 2019/2/26

N2 - 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.

AB - 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.

KW - Bioenergetics

KW - Catalytic intermediates

KW - Complex IV

KW - Crystallography

KW - X-ray free electron laser

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AN - SCOPUS:85062011056

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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

Abstract

Keywords

ASJC Scopus subject areas

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Time-resolved SFX structure of the PR intermediate of cytochrome c oxidase at room temperature

SFX structure of reduced cytochrome c oxidase at room temperature

SFX structure of oxidized cytochrome c oxidase at room temperature

Cite this

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

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Datasets

Time-resolved SFX structure of the PR intermediate of cytochrome c oxidase at room temperature

SFX structure of reduced cytochrome c oxidase at room temperature

SFX structure of oxidized cytochrome c oxidase at room temperature

Cite this