Oxygen-evolving photosystem II structures during S1–S2–S3 transitions
Author:
Li HongjieORCID, Nakajima YoshikiORCID, Nango ErikoORCID, Owada Shigeki, Yamada Daichi, Hashimoto Kana, Luo Fangjia, Tanaka Rie, Akita FusamichiORCID, Kato Koji, Kang JungminORCID, Saitoh YasunoriORCID, Kishi Shunpei, Yu Huaxin, Matsubara Naoki, Fujii Hajime, Sugahara Michihiro, Suzuki Mamoru, Masuda Tetsuya, Kimura TetsunariORCID, Thao Tran NguyenORCID, Yonekura Shinichiro, Yu Long-JiangORCID, Tosha TakehikoORCID, Tono KensukeORCID, Joti YasumasaORCID, Hatsui TakakiORCID, Yabashi MakinaORCID, Kubo MinoruORCID, Iwata SoORCID, Isobe Hiroshi, Yamaguchi Kizashi, Suga MichihiroORCID, Shen Jian-RenORCID
Abstract
AbstractPhotosystem 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.
Publisher
Springer Science and Business Media LLC
Subject
Multidisciplinary
Reference69 articles.
1. Kok, B., Forbush, B. & McGloin, M. Cooperation of charges in photosynthetic O2 evolution–I. A linear four step mechanism. Photochem. Photobiol. 11, 457–475 (1970). 2. Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60 (2011). 3. Suga, M. et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103 (2015). 4. Suga, M. et al. Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543, 131–135 (2017). 5. Kern, J. et al. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature 563, 421–424 (2018).
|
|