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XFEL structure of cyanobacterial photosystem II following two flashes (2F) with a 200-microsecond delay
Structural highlights
FunctionPSBA_THEVL D1 (PsbA) and D2 (PsbD) bind P680, the primary electron donor of photosystem II (PSII) as well as electron acceptors. PSII is a light-driven water plastoquinone oxidoreductase, using light energy to abstract electrons from H(2)O, generating a proton gradient subsequently used for ATP formation.[HAMAP-Rule:MF_01379] Publication Abstract from PubMedPhotosystem II (PSII) catalyses the oxidation of water through a four-step cycle of S(i) states (i = 0-4) at the Mn(4)CaO(5) 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 Mn(4)CaO(5) 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 Ca(2+) 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. Oxygen-evolving photosystem II structures during S(1)-S(2)-S(3) transitions.,Li H, Nakajima Y, Nango E, Owada S, Yamada D, Hashimoto K, Luo F, Tanaka R, Akita F, Kato K, Kang J, Saitoh Y, Kishi S, Yu H, Matsubara N, Fujii H, Sugahara M, Suzuki M, Masuda T, Kimura T, Thao TN, Yonekura S, Yu LJ, Tosha T, Tono K, Joti Y, Hatsui T, Yabashi M, Kubo M, Iwata S, Isobe H, Yamaguchi K, Suga M, Shen JR Nature. 2024 Feb;626(7999):670-677. doi: 10.1038/s41586-023-06987-5. Epub 2024 , Jan 31. PMID:38297122[1] From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine. References
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