Oxygen-evolving photosystem II structures during S1–S2–S3 transitions

Hongjie Li, Yoshiki Nakajima, Eriko Nango, Shigeki Owada, Daichi Yamada, Kana Hashimoto, Fangjia Luo, Rie Tanaka, Fusamichi Akita, Koji Kato, Jungmin Kang, Yasunori Saitoh, Shunpei Kishi, Huaxin Yu, Naoki Matsubara, Hajime Fujii, Michihiro Sugahara, Mamoru Suzuki, Tetsuya Masuda, Tetsunari Kimura, Tran Nguyen Thao, Shinichiro Yonekura, Long-Jiang Yu, Takehiko Tosha, Kensuke Tono, Yasumasa Joti, Takaki Hatsui, Makina Yabashi, Minoru Kubo, So Iwata, Hiroshi Isobe, Kizashi Yamaguchi, Michihiro Suga () and Jian-Ren Shen ()
Additional contact information
Hongjie Li: Okayama University
Yoshiki Nakajima: Okayama University
Eriko Nango: Tohoku University
Shigeki Owada: Japan Synchrotron Radiation Research Institute
Daichi Yamada: University of Hyogo
Kana Hashimoto: Okayama University
Fangjia Luo: Japan Synchrotron Radiation Research Institute
Rie Tanaka: RIKEN SPring-8 Center
Fusamichi Akita: Okayama University
Koji Kato: Okayama University
Jungmin Kang: RIKEN SPring-8 Center
Yasunori Saitoh: Okayama University
Shunpei Kishi: Okayama University
Huaxin Yu: Okayama University
Naoki Matsubara: Okayama University
Hajime Fujii: Okayama University
Michihiro Sugahara: Japan Synchrotron Radiation Research Institute
Mamoru Suzuki: Osaka University
Tetsuya Masuda: Ryukoku University
Tetsunari Kimura: Kobe University
Tran Nguyen Thao: Okayama University
Shinichiro Yonekura: Okayama University
Long-Jiang Yu: 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: University of Hyogo
So Iwata: RIKEN SPring-8 Center
Hiroshi Isobe: Okayama University
Kizashi Yamaguchi: Osaka University
Michihiro Suga: Okayama University
Jian-Ren Shen: Okayama University

Nature, 2024, vol. 626, issue 7999, 670-677

Abstract: Abstract Photosystem II (PSII) catalyses the oxidation of water through a four-step cycle of Si states (i = 0–4) at the Mn4CaO5 cluster1–3, during which an extra oxygen (O6) is incorporated at the S3 state to form a possible dioxygen4–7. 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.

Date: 2024
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DOI: 10.1038/s41586-023-06987-5

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