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

Abstract

Photosystem II (PSII) catalyses the oxidation of water through a four-step cycle of Si states (i = 0–4) at the Mn4CaO5 cluster during which an extra oxygen (O6) is incorporated at the S3 state to form a possible dioxygen. 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.
*This text is adapted from the following paper.

Paper Information

Journal

Nature

Title

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

DOI

10.1038/s41586-023-06987-5

Author

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, Jian-Ren Shen

Published

January 31, 2024

URL

https://www.nature.com/articles/s41586-023-06987-5

Contact

Minoru Kubo
Graduate School of Science
University of Hyogo

E-mail

minoru[at]sci.u-hyogo.ac.jp
*Please change [at] to @.

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