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Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition

Light-driven oxidation of water to molecular oxygen is catalyzed by the oxygen-evolving complex (OEC) in Photosystem II (PS II). This multi-electron, multi-proton catalysis requires the transport of two water molecules to and four protons from the OEC. A high-resolution 1.89 Å structure obtained by...

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Autores principales: Hussein, Rana, Ibrahim, Mohamed, Bhowmick, Asmit, Simon, Philipp S., Chatterjee, Ruchira, Lassalle, Louise, Doyle, Margaret, Bogacz, Isabel, Kim, In-Sik, Cheah, Mun Hon, Gul, Sheraz, de Lichtenberg, Casper, Chernev, Petko, Pham, Cindy C., Young, Iris D., Carbajo, Sergio, Fuller, Franklin D., Alonso-Mori, Roberto, Batyuk, Alex, Sutherlin, Kyle D., Brewster, Aaron S., Bolotovsky, Robert, Mendez, Derek, Holton, James M., Moriarty, Nigel W., Adams, Paul D., Bergmann, Uwe, Sauter, Nicholas K., Dobbek, Holger, Messinger, Johannes, Zouni, Athina, Kern, Jan, Yachandra, Vittal K., Yano, Junko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585918/
https://www.ncbi.nlm.nih.gov/pubmed/34764256
http://dx.doi.org/10.1038/s41467-021-26781-z
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author Hussein, Rana
Ibrahim, Mohamed
Bhowmick, Asmit
Simon, Philipp S.
Chatterjee, Ruchira
Lassalle, Louise
Doyle, Margaret
Bogacz, Isabel
Kim, In-Sik
Cheah, Mun Hon
Gul, Sheraz
de Lichtenberg, Casper
Chernev, Petko
Pham, Cindy C.
Young, Iris D.
Carbajo, Sergio
Fuller, Franklin D.
Alonso-Mori, Roberto
Batyuk, Alex
Sutherlin, Kyle D.
Brewster, Aaron S.
Bolotovsky, Robert
Mendez, Derek
Holton, James M.
Moriarty, Nigel W.
Adams, Paul D.
Bergmann, Uwe
Sauter, Nicholas K.
Dobbek, Holger
Messinger, Johannes
Zouni, Athina
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
author_facet Hussein, Rana
Ibrahim, Mohamed
Bhowmick, Asmit
Simon, Philipp S.
Chatterjee, Ruchira
Lassalle, Louise
Doyle, Margaret
Bogacz, Isabel
Kim, In-Sik
Cheah, Mun Hon
Gul, Sheraz
de Lichtenberg, Casper
Chernev, Petko
Pham, Cindy C.
Young, Iris D.
Carbajo, Sergio
Fuller, Franklin D.
Alonso-Mori, Roberto
Batyuk, Alex
Sutherlin, Kyle D.
Brewster, Aaron S.
Bolotovsky, Robert
Mendez, Derek
Holton, James M.
Moriarty, Nigel W.
Adams, Paul D.
Bergmann, Uwe
Sauter, Nicholas K.
Dobbek, Holger
Messinger, Johannes
Zouni, Athina
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
author_sort Hussein, Rana
collection PubMed
description Light-driven oxidation of water to molecular oxygen is catalyzed by the oxygen-evolving complex (OEC) in Photosystem II (PS II). This multi-electron, multi-proton catalysis requires the transport of two water molecules to and four protons from the OEC. A high-resolution 1.89 Å structure obtained by averaging all the S states and refining the data of various time points during the S(2) to S(3) transition has provided better visualization of the potential pathways for substrate water insertion and proton release. Our results indicate that the O1 channel is the likely water intake pathway, and the Cl1 channel is the likely proton release pathway based on the structural rearrangements of water molecules and amino acid side chains along these channels. In particular in the Cl1 channel, we suggest that residue D1-E65 serves as a gate for proton transport by minimizing the back reaction. The results show that the water oxidation reaction at the OEC is well coordinated with the amino acid side chains and the H-bonding network over the entire length of the channels, which is essential in shuttling substrate waters and protons.
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spelling pubmed-85859182021-11-15 Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition Hussein, Rana Ibrahim, Mohamed Bhowmick, Asmit Simon, Philipp S. Chatterjee, Ruchira Lassalle, Louise Doyle, Margaret Bogacz, Isabel Kim, In-Sik Cheah, Mun Hon Gul, Sheraz de Lichtenberg, Casper Chernev, Petko Pham, Cindy C. Young, Iris D. Carbajo, Sergio Fuller, Franklin D. Alonso-Mori, Roberto Batyuk, Alex Sutherlin, Kyle D. Brewster, Aaron S. Bolotovsky, Robert Mendez, Derek Holton, James M. Moriarty, Nigel W. Adams, Paul D. Bergmann, Uwe Sauter, Nicholas K. Dobbek, Holger Messinger, Johannes Zouni, Athina Kern, Jan Yachandra, Vittal K. Yano, Junko Nat Commun Article Light-driven oxidation of water to molecular oxygen is catalyzed by the oxygen-evolving complex (OEC) in Photosystem II (PS II). This multi-electron, multi-proton catalysis requires the transport of two water molecules to and four protons from the OEC. A high-resolution 1.89 Å structure obtained by averaging all the S states and refining the data of various time points during the S(2) to S(3) transition has provided better visualization of the potential pathways for substrate water insertion and proton release. Our results indicate that the O1 channel is the likely water intake pathway, and the Cl1 channel is the likely proton release pathway based on the structural rearrangements of water molecules and amino acid side chains along these channels. In particular in the Cl1 channel, we suggest that residue D1-E65 serves as a gate for proton transport by minimizing the back reaction. The results show that the water oxidation reaction at the OEC is well coordinated with the amino acid side chains and the H-bonding network over the entire length of the channels, which is essential in shuttling substrate waters and protons. Nature Publishing Group UK 2021-11-11 /pmc/articles/PMC8585918/ /pubmed/34764256 http://dx.doi.org/10.1038/s41467-021-26781-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hussein, Rana
Ibrahim, Mohamed
Bhowmick, Asmit
Simon, Philipp S.
Chatterjee, Ruchira
Lassalle, Louise
Doyle, Margaret
Bogacz, Isabel
Kim, In-Sik
Cheah, Mun Hon
Gul, Sheraz
de Lichtenberg, Casper
Chernev, Petko
Pham, Cindy C.
Young, Iris D.
Carbajo, Sergio
Fuller, Franklin D.
Alonso-Mori, Roberto
Batyuk, Alex
Sutherlin, Kyle D.
Brewster, Aaron S.
Bolotovsky, Robert
Mendez, Derek
Holton, James M.
Moriarty, Nigel W.
Adams, Paul D.
Bergmann, Uwe
Sauter, Nicholas K.
Dobbek, Holger
Messinger, Johannes
Zouni, Athina
Kern, Jan
Yachandra, Vittal K.
Yano, Junko
Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title_full Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title_fullStr Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title_full_unstemmed Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title_short Structural dynamics in the water and proton channels of photosystem II during the S(2) to S(3) transition
title_sort structural dynamics in the water and proton channels of photosystem ii during the s(2) to s(3) transition
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585918/
https://www.ncbi.nlm.nih.gov/pubmed/34764256
http://dx.doi.org/10.1038/s41467-021-26781-z
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