Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography

The water oxidation reaction in photosystem II (PS II) produces most of the molecular oxygen in the atmosphere, which sustains life on Earth, and in this process releases four electrons and four protons that drive the downstream process of CO(2) fixation in the photosynthetic apparatus. The catalyti...

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Autores principales: Bhowmick, Asmit, Simon, Philipp S., Bogacz, Isabel, Hussein, Rana, Zhang, Miao, Makita, Hiroki, Ibrahim, Mohamed, Chatterjee, Ruchira, Doyle, Margaret D., Cheah, Mun Hon, Chernev, Petko, Fuller, Franklin D., Fransson, Thomas, Alonso-Mori, Roberto, Brewster, Aaron S., Sauter, Nicholas K., Bergmann, Uwe, Dobbek, Holger, Zouni, Athina, Messinger, Johannes, Kern, Jan, Yachandra, Vittal K., Yano, Junko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: International Union of Crystallography 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619448/
https://www.ncbi.nlm.nih.gov/pubmed/37870936
http://dx.doi.org/10.1107/S2052252523008928
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author Bhowmick, Asmit
Simon, Philipp S.
Bogacz, Isabel
Hussein, Rana
Zhang, Miao
Makita, Hiroki
Ibrahim, Mohamed
Chatterjee, Ruchira
Doyle, Margaret D.
Cheah, Mun Hon
Chernev, Petko
Fuller, Franklin D.
Fransson, Thomas
Alonso-Mori, Roberto
Brewster, Aaron S.
Sauter, Nicholas K.
Bergmann, Uwe
Dobbek, Holger
Zouni, Athina
Messinger, Johannes
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
author_facet Bhowmick, Asmit
Simon, Philipp S.
Bogacz, Isabel
Hussein, Rana
Zhang, Miao
Makita, Hiroki
Ibrahim, Mohamed
Chatterjee, Ruchira
Doyle, Margaret D.
Cheah, Mun Hon
Chernev, Petko
Fuller, Franklin D.
Fransson, Thomas
Alonso-Mori, Roberto
Brewster, Aaron S.
Sauter, Nicholas K.
Bergmann, Uwe
Dobbek, Holger
Zouni, Athina
Messinger, Johannes
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
author_sort Bhowmick, Asmit
collection PubMed
description The water oxidation reaction in photosystem II (PS II) produces most of the molecular oxygen in the atmosphere, which sustains life on Earth, and in this process releases four electrons and four protons that drive the downstream process of CO(2) fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn(4)Ca complex (Mn(4)CaO(5)) which is progressively oxidized upon the absorption of light by the chloro­phyll of the PS II reaction center, and the accumulation of four oxidative equivalents in the catalytic center results in the oxidation of two waters to di­oxy­gen in the last step. The recent emergence of X-ray free-electron lasers (XFELs) with intense femtosecond X-ray pulses has opened up opportunities to visualize this reaction in PS II as it proceeds through the catalytic cycle. In this review, we summarize our recent studies of the catalytic reaction in PS II by following the structural changes along the reaction pathway via room-temperature X-ray crystallography using XFELs. The evolution of the electron density changes at the Mn complex reveals notable structural changes, including the insertion of O(X) from a new water molecule, which disappears on completion of the reaction, implicating it in the O—O bond formation reaction. We were also able to follow the structural dynamics of the protein coordinating with the catalytic complex and of channels within the protein that are important for substrate and product transport, revealing well orchestrated conformational changes in response to the electronic changes at the Mn(4)Ca cluster.
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spelling pubmed-106194482023-11-02 Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography Bhowmick, Asmit Simon, Philipp S. Bogacz, Isabel Hussein, Rana Zhang, Miao Makita, Hiroki Ibrahim, Mohamed Chatterjee, Ruchira Doyle, Margaret D. Cheah, Mun Hon Chernev, Petko Fuller, Franklin D. Fransson, Thomas Alonso-Mori, Roberto Brewster, Aaron S. Sauter, Nicholas K. Bergmann, Uwe Dobbek, Holger Zouni, Athina Messinger, Johannes Kern, Jan Yachandra, Vittal K. Yano, Junko IUCrJ Topical Reviews The water oxidation reaction in photosystem II (PS II) produces most of the molecular oxygen in the atmosphere, which sustains life on Earth, and in this process releases four electrons and four protons that drive the downstream process of CO(2) fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn(4)Ca complex (Mn(4)CaO(5)) which is progressively oxidized upon the absorption of light by the chloro­phyll of the PS II reaction center, and the accumulation of four oxidative equivalents in the catalytic center results in the oxidation of two waters to di­oxy­gen in the last step. The recent emergence of X-ray free-electron lasers (XFELs) with intense femtosecond X-ray pulses has opened up opportunities to visualize this reaction in PS II as it proceeds through the catalytic cycle. In this review, we summarize our recent studies of the catalytic reaction in PS II by following the structural changes along the reaction pathway via room-temperature X-ray crystallography using XFELs. The evolution of the electron density changes at the Mn complex reveals notable structural changes, including the insertion of O(X) from a new water molecule, which disappears on completion of the reaction, implicating it in the O—O bond formation reaction. We were also able to follow the structural dynamics of the protein coordinating with the catalytic complex and of channels within the protein that are important for substrate and product transport, revealing well orchestrated conformational changes in response to the electronic changes at the Mn(4)Ca cluster. International Union of Crystallography 2023-10-24 /pmc/articles/PMC10619448/ /pubmed/37870936 http://dx.doi.org/10.1107/S2052252523008928 Text en © Asmit Bhowmick et al. 2023 https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution (CC-BY) Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are cited.
spellingShingle Topical Reviews
Bhowmick, Asmit
Simon, Philipp S.
Bogacz, Isabel
Hussein, Rana
Zhang, Miao
Makita, Hiroki
Ibrahim, Mohamed
Chatterjee, Ruchira
Doyle, Margaret D.
Cheah, Mun Hon
Chernev, Petko
Fuller, Franklin D.
Fransson, Thomas
Alonso-Mori, Roberto
Brewster, Aaron S.
Sauter, Nicholas K.
Bergmann, Uwe
Dobbek, Holger
Zouni, Athina
Messinger, Johannes
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title_full Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title_fullStr Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title_full_unstemmed Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title_short Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
title_sort going around the kok cycle of the water oxidation reaction with femtosecond x-ray crystallography
topic Topical Reviews
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619448/
https://www.ncbi.nlm.nih.gov/pubmed/37870936
http://dx.doi.org/10.1107/S2052252523008928
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