Structural evidence for intermediates during O2 formation in photosystem II

Asmit Bhowmick, Rana Hussein, Isabel Bogacz, Philipp S. Simon, Mohamed Ibrahim, Ruchira Chatterjee, Margaret D. Doyle, Mun Hon Cheah, Thomas Fransson, Petko Chernev, In-Sik Kim, Hiroki Makita, Medhanjali Dasgupta, Corey J. Kaminsky, Miao Zhang, Julia Gätcke, Stephanie Haupt, Isabela I. Nangca, Stephen M. Keable, A. Orkun Aydin, Kensuke Tono, Shigeki Owada, Leland B. Gee, Franklin D. Fuller, Alexander Batyuk, Roberto Alonso-Mori, James M. Holton, Daniel W. Paley, Nigel W. Moriarty, Fikret Mamedov, Paul D. Adams, Aaron S. Brewster, Holger Dobbek, Nicholas K. Sauter, Uwe Bergmann, Athina Zouni (), Johannes Messinger (), Jan Kern, Junko Yano () and Vittal K. Yachandra ()
Additional contact information
Asmit Bhowmick: Lawrence Berkeley National Laboratory
Rana Hussein: Humboldt Universität zu Berlin
Isabel Bogacz: Lawrence Berkeley National Laboratory
Philipp S. Simon: Lawrence Berkeley National Laboratory
Mohamed Ibrahim: Humboldt Universität zu Berlin
Ruchira Chatterjee: Lawrence Berkeley National Laboratory
Margaret D. Doyle: Lawrence Berkeley National Laboratory
Mun Hon Cheah: Uppsala University
Thomas Fransson: KTH Royal Institute of Technology
Petko Chernev: Uppsala University
In-Sik Kim: Lawrence Berkeley National Laboratory
Hiroki Makita: Lawrence Berkeley National Laboratory
Medhanjali Dasgupta: Lawrence Berkeley National Laboratory
Corey J. Kaminsky: Lawrence Berkeley National Laboratory
Miao Zhang: Lawrence Berkeley National Laboratory
Julia Gätcke: Humboldt Universität zu Berlin
Stephanie Haupt: Humboldt Universität zu Berlin
Isabela I. Nangca: Lawrence Berkeley National Laboratory
Stephen M. Keable: Lawrence Berkeley National Laboratory
A. Orkun Aydin: Uppsala University
Kensuke Tono: Japan Synchrotron Radiation Research Institute
Shigeki Owada: Japan Synchrotron Radiation Research Institute
Leland B. Gee: SLAC National Accelerator Laboratory
Franklin D. Fuller: SLAC National Accelerator Laboratory
Alexander Batyuk: SLAC National Accelerator Laboratory
Roberto Alonso-Mori: SLAC National Accelerator Laboratory
James M. Holton: Lawrence Berkeley National Laboratory
Daniel W. Paley: Lawrence Berkeley National Laboratory
Nigel W. Moriarty: Lawrence Berkeley National Laboratory
Fikret Mamedov: Uppsala University
Paul D. Adams: Lawrence Berkeley National Laboratory
Aaron S. Brewster: Lawrence Berkeley National Laboratory
Holger Dobbek: Humboldt Universität zu Berlin
Nicholas K. Sauter: Lawrence Berkeley National Laboratory
Uwe Bergmann: University of Wisconsin–Madison
Athina Zouni: Humboldt Universität zu Berlin
Johannes Messinger: Uppsala University
Jan Kern: Lawrence Berkeley National Laboratory
Junko Yano: Lawrence Berkeley National Laboratory
Vittal K. Yachandra: Lawrence Berkeley National Laboratory

Nature, 2023, vol. 617, issue 7961, 629-636

Abstract: Abstract In natural photosynthesis, the light-driven splitting of water into electrons, protons and molecular oxygen forms the first step of the solar-to-chemical energy conversion process. The reaction takes place in photosystem II, where the Mn4CaO5 cluster first stores four oxidizing equivalents, the S0 to S4 intermediate states in the Kok cycle, sequentially generated by photochemical charge separations in the reaction center and then catalyzes the O–O bond formation chemistry1–3. Here, we report room temperature snapshots by serial femtosecond X-ray crystallography to provide structural insights into the final reaction step of Kok’s photosynthetic water oxidation cycle, the S3→[S4]→S0 transition where O2 is formed and Kok’s water oxidation clock is reset. Our data reveal a complex sequence of events, which occur over micro- to milliseconds, comprising changes at the Mn4CaO5 cluster, its ligands and water pathways as well as controlled proton release through the hydrogen-bonding network of the Cl1 channel. Importantly, the extra O atom Ox, which was introduced as a bridging ligand between Ca and Mn1 during the S2→S3 transition4–6, disappears or relocates in parallel with Yz reduction starting at approximately 700 μs after the third flash. The onset of O2 evolution, as indicated by the shortening of the Mn1–Mn4 distance, occurs at around 1,200 μs, signifying the presence of a reduced intermediate, possibly a bound peroxide.

Date: 2023
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DOI: 10.1038/s41586-023-06038-z

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