Structural evidence for intermediates during O2 formation in photosystem II

Bhowmick, Asmit; Hussein, Rana; Bogacz, Isabel; Simon, Philipp S.; Ibrahim, Mohamed; Chatterjee, Ruchira; Doyle, Margaret D.; Cheah, Mun Hon; Fransson, Thomas; Chernev, Petko; Kim, In-Sik; Makita, Hiroki; Dasgupta, Medhanjali; Kaminsky, Corey J.; Zhang, Miao; Gätcke, Julia; Haupt, Stephanie; Nangca, Isabela I.; Keable, Stephen M.; Aydin, A. Orkun; Tono, Kensuke; Owada, Shigeki; Gee, Leland B.; Fuller, Franklin D.; Batyuk, Alexander; Alonso-Mori, Roberto; Holton, James M.; Paley, Daniel W.; Moriarty, Nigel W.; Mamedov, Fikret; Adams, Paul D.; Brewster, Aaron S.; Dobbek, Holger; Sauter, Nicholas K.; Bergmann, Uwe; Zouni, Athina; Messinger, Johannes; Kern, Jan; Yano, Junko; Yachandra, Vittal K.

doi:10.1038/s41586-023-06038-z

Title: Structural evidence for intermediates during O₂ formation in photosystem II

Journal Article · 03 May 2023 · Nature (London)

DOI: https://doi.org/10.1038/s41586-023-06038-z · OSTI ID:2001435

^[1];

^[2]; Bogacz, Isabel ^[1];

^[1]; Ibrahim, Mohamed ^[2]; Chatterjee, Ruchira ^[1]; Doyle, Margaret D. ^[1];

^[3]; Fransson, Thomas ^[4]; Chernev, Petko ^[3]; Kim, In-Sik ^[1];

^[1]; Dasgupta, Medhanjali ^[1]; Kaminsky, Corey J. ^[1]; Zhang, Miao ^[1]; Gätcke, Julia ^[2]; Haupt, Stephanie ^[2];

^[1]; Keable, Stephen M. ^[1];

^[3] more »

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Humboldt Univ. of Berlin (Germany)
Uppsala Univ. (Sweden)
KTH Royal Inst. of Technology, Stockholm (Sweden)
Japan Synchrotron Radiation Research Institute, Sayo, Hyogo (Japan); RIKEN SPring-8 Center, Sayo (Japan)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, San Francisco, CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of Wisconsin, Madison, WI (United States)
Uppsala Univ. (Sweden); Umea Univ. (Sweden)

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 chemistry. 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 O_x, which was introduced as a bridging ligand between Ca and Mn1 during the S₂→S₃ transition disappears or relocates in parallel with Y_z 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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); National Institutes of Health (NIH); USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-76SF00515; AC02-05CH11231

OSTI ID:: 2001435

Alternate ID(s):: OSTI ID: 2228868

Journal Information:: Nature (London), Vol. 617, Issue 7961; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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