Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition
Abstract
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 S2 to S3 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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- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institutes of Health (NIH); Exascale Computing Project; Caroline von Humboldt Stipendium; German Research Foundation (DFG); USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1829937
- Alternate Identifier(s):
- OSTI ID: 1855199; OSTI ID: 1869819
- Grant/Contract Number:
- AC02-05CH11231; AC02-76SF00515; GM055302; GM110501; GM126289; GM117126; 17-SC20-SC; GM133081; GM124149; GM124169; S10 OD023453
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 12 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; bioenergetics; structural biology; x-ray crystallography
Citation Formats
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., and Yano, Junko. Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition. United Kingdom: N. p., 2021.
Web. doi:10.1038/s41467-021-26781-z.
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 S2 to S3 transition. United Kingdom. https://doi.org/10.1038/s41467-021-26781-z
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., and Yano, Junko. Thu .
"Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition". United Kingdom. https://doi.org/10.1038/s41467-021-26781-z.
@article{osti_1829937,
title = {Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition},
author = {Hussein, Rana and Ibrahim, Mohamed and Bhowmick, Asmit and Simon, Philipp S. and Chatterjee, Ruchira and Lassalle, Louise and Doyle, Margaret and Bogacz, Isabel and Kim, In-Sik and Cheah, Mun Hon and Gul, Sheraz and de Lichtenberg, Casper and Chernev, Petko and Pham, Cindy C. and Young, Iris D. and Carbajo, Sergio and Fuller, Franklin D. and Alonso-Mori, Roberto and Batyuk, Alex and Sutherlin, Kyle D. and Brewster, Aaron S. and Bolotovsky, Robert and Mendez, Derek and Holton, James M. and Moriarty, Nigel W. and Adams, Paul D. and Bergmann, Uwe and Sauter, Nicholas K. and Dobbek, Holger and Messinger, Johannes and Zouni, Athina and Kern, Jan and Yachandra, Vittal K. and Yano, Junko},
abstractNote = {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 S2 to S3 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.},
doi = {10.1038/s41467-021-26781-z},
journal = {Nature Communications},
number = 1,
volume = 12,
place = {United Kingdom},
year = {2021},
month = {11}
}
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