Springer Science and Business Media LLC Acta Medica Okayama 0028-0836 626 7999 2024 Oxygen-evolving photosystem II structures during S1–S2–S3 transitions 670 677 EN Hongjie Li Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Yoshiki Nakajima Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Eriko Nango Institute of Multidisciplinary Research for Advanced Materials, Tohoku University Shigeki Owada Japan Synchrotron Radiation Research Institute Daichi Yamada Department of Picobiology, Graduate School of Life Science, University of Hyogo Kana Hashimoto Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Fangjia Luo Japan Synchrotron Radiation Research Institute Rie Tanaka RIKEN SPring-8 Center Fusamichi Akita Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Koji Kato Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Jungmin Kang RIKEN SPring-8 Center Yasunori Saitoh Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Shunpei Kishi Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Huaxin Yu Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Naoki Matsubara Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Hajime Fujii Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Michihiro Sugahara Japan Synchrotron Radiation Research Institute Mamoru Suzuki Institute for Protein Research, Osaka University Tetsuya Masuda Division of Food and Nutrition, Faculty of Agriculture, Ryukoku University Tetsunari Kimura Department of Chemistry, Graduate School of Science, Kobe University Tran Nguyen Thao Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Shinichiro Yonekura Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Long-Jiang Yu Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Takehiko Tosha RIKEN SPring-8 Center Kensuke Tono Japan Synchrotron Radiation Research Institute Yasumasa Joti Japan Synchrotron Radiation Research Institute Takaki Hatsui Japan Synchrotron Radiation Research Institute Makina Yabashi Japan Synchrotron Radiation Research Institute Minoru Kubo Department of Picobiology, Graduate School of Life Science, University of Hyogo So Iwata RIKEN SPring-8 Center Hiroshi Isobe Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Kizashi Yamaguchi Center for Quantum Information and Quantum Biology, Osaka University Michihiro Suga Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Jian-Ren Shen Research Institute for Interdisciplinary Science, Graduate School of Natural Science and Technology, Okayama University Photosystem II (PSII) catalyses the oxidation of water through a four-step cycle of Si states (i = 0–4) at the Mn4CaO5 cluster1,2,3, during which an extra oxygen (O6) is incorporated at the S3 state to form a possible dioxygen4,5,6,7. Structural changes of the metal cluster and its environment during the S-state transitions have been studied on the microsecond timescale. Here we use pump-probe serial femtosecond crystallography to reveal the structural dynamics of PSII from nanoseconds to milliseconds after illumination with one flash (1F) or two flashes (2F). YZ, a tyrosine residue that connects the reaction centre P680 and the Mn4CaO5 cluster, showed structural changes on a nanosecond timescale, as did its surrounding amino acid residues and water molecules, reflecting the fast transfer of electrons and protons after flash illumination. Notably, one water molecule emerged in the vicinity of Glu189 of the D1 subunit of PSII (D1-E189), and was bound to the Ca2+ ion on a sub-microsecond timescale after 2F illumination. This water molecule disappeared later with the concomitant increase of O6, suggesting that it is the origin of O6. We also observed concerted movements of water molecules in the O1, O4 and Cl-1 channels and their surrounding amino acid residues to complete the sequence of electron transfer, proton release and substrate water delivery. These results provide crucial insights into the structural dynamics of PSII during S-state transitions as well as O–O bond formation. No potential conflict of interest relevant to this article was reported.

American Association for the Advancement of Science Acta Medica Okayama 0036-8075 366 6463 2019 An oxyl/oxo mechanism for dioxygen bond formation in PSII revealed by X-ray free electron lasers 334 338 EN Michihiro Suga Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Fusamichi Akita Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Keitaro Yamashita RIKEN SPring-8 Center Yoshiki Nakajima Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Go Ueno RIKEN SPring-8 Center Hongjie Li Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Takahiro Yamane Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Kunio Hirata RIKEN SPring-8 Center Yasufumi Umena Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Shinichiro Yonekura Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Long-Jiang Yu Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Hironori Murakami Japan Synchrotron Radiation Research Institute Takashi Nomura RIKEN SPring-8 Center Tetsunari Kimura Department of Chemistry, Graduate School of Science, Kobe University Minoru Kubo RIKEN SPring-8 Center Seiki Baba Japan Synchrotron Radiation Research Institute Takashi Kumasaka Japan Synchrotron Radiation Research Institute Kensuke Tono RIKEN SPring-8 Center Makina Yabashi RIKEN SPring-8 Center Hiroshi Isobe Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Kizashi Yamaguchi The Institute for Scientific and Industrial Research, Osaka University Masaki Yamamoto RIKEN SPring-8 Center Hideo Ago RIKEN SPring-8 Center Jian-Ren Shen Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University Photosynthetic water oxidation is catalyzed by the Mn4CaO5 cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S0 to S4). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S1, S2, and S3 states by x-ray free-electron laser serial crystallography. No insertion of water was found in S2, but flipping of D1 Glu189 upon transition to S3 leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn4CaO6 cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reveal cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation. No potential conflict of interest relevant to this article was reported.