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

• 成果类型: Article
• 署名作者: Li, Hongjie; Nakajima, Yoshiki; Nango, Eriko; Owada, Shigeki; Yamada, Daichi; Hashimoto, Kana; Luo, Fangjia; Tanaka, Rie; Akita, Fusamichi; Kato, Koji; Kang, Jungmin; Saitoh, Yasunori; Kishi, Shunpei; Yu, Huaxin; Matsubara, Naoki; Fujii, Hajime; Sugahara, Michihiro; Suzuki, Mamoru; Masuda, Tetsuya; Kimura, Tetsunari; Thao, Tran Nguyen; Yonekura, Shinichiro; Yu, Long-Jiang; Tosha, Takehiko; Tono, Kensuke; Joti, Yasumasa; Hatsui, Takaki; Yabashi, Makina; Kubo, Minoru; Iwata, So; Isobe, Hiroshi; Yamaguchi, Kizashi; Suga, Michihiro; Shen, Jian-Ren
• 署名单位: Okayama University; Tohoku University; RIKEN; Japan Synchrotron Radiation Research Institute; University of Hyogo; Kyoto University; University of Osaka; Ryukoku University; Kobe University; Chinese Academy of Sciences; Institute of Botany, CAS; University of Osaka
• 刊物名称: Nature
• ISSN/ISSBN: 0028-5082
• DOI: 10.1038/s41586-023-06987-5
• 发表日期: 2024-02-15
• 页码: 670-+
• 关键词: serial femtosecond crystallography; photosynthetic water oxidation; effective core potentials; difference spectroscopy; molecular calculations; proton-transfer; electron; complex; binding; mechanism

摘要

Photosystem II (PSII) catalyses the oxidation of water through a four-step cycle of S-i states (i=0-4) at the Mn4CaO5 cluster(1-3), during which an extra oxygen (O6) is incorporated at the S-3 state to form a possible dioxygen(4-7). 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). Y-Z, 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.