title: Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.
abstract: Photosynthesis converts light energy into biologically useful chemical energy vital to life on Earth. The initial reaction of photosynthesis takes place in photosystem II (PSII), a 700-kilodalton homodimeric membrane protein complex that catalyses photo-oxidation of water into dioxygen through an S-state cycle of the oxygen evolving complex (OEC). The structure of PSII has been solved by X-ray diffraction (XRD) at 1.9 ångström resolution, which revealed that the OEC is a Mn4CaO5-cluster coordinated by a well defined protein environment. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation, and slight differences were found in the Mn-Mn distances determined by XRD, EXAFS and theoretical studies. Here we report a 'radiation-damage-free' structure of PSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 ångströms using femtosecond X-ray pulses of the SPring-8 ångström compact free-electron laser (SACLA) and hundreds of large, highly isomorphous PSII crystals. Compared with the structure from XRD, the OEC in the X-ray free electron laser structure has Mn-Mn distances that are shorter by 0.1-0.2 ångströms. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) and Mn4A(III), based on the average Mn-ligand distances and analysis of the Jahn-Teller axis on Mn(III). One of the oxo-bridged oxygens, O5, has significantly longer distances to Mn than do the other oxo-oxygen atoms, suggesting that O5 is a hydroxide ion instead of a normal oxygen dianion and therefore may serve as one of the substrate oxygen atoms. These findings provide a structural basis for the mechanism of oxygen evolution, and we expect that this structure will provide a blueprint for the design of artificial catalysts for water oxidation.
authors.affiliation: Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan.
authors.forename: Michihiro
authors.initials: M
authors.lastname: Suga
authors.affiliation: Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan.
authors.forename: Fusamichi
authors.initials: F
authors.lastname: Akita
authors.affiliation: 1] RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan [2] Japan Science and Technology Agency (JST), Core Research for Evolutional Science and Technology (CREST), Kawaguchi, Saitama 332-0012, Japan.
authors.forename: Kunio
authors.initials: K
authors.lastname: Hirata
authors.affiliation: RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan.
authors.forename: Go
authors.initials: G
authors.lastname: Ueno
authors.affiliation: RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan.
authors.forename: Hironori
authors.initials: H
authors.lastname: Murakami
authors.affiliation: Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan.
authors.forename: Yoshiki
authors.initials: Y
authors.lastname: Nakajima
authors.affiliation: Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan.
authors.forename: Tetsuya
authors.initials: T
authors.lastname: Shimizu
authors.affiliation: RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan.
authors.forename: Keitaro
authors.initials: K
authors.lastname: Yamashita
authors.affiliation: RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan.
authors.forename: Masaki
authors.initials: M
authors.lastname: Yamamoto
authors.affiliation: RIKEN SPring-8 Center, 1-1-1 Kouto Sayo, Hyogo 679-5148, Japan.
authors.forename: Hideo
authors.initials: H
authors.lastname: Ago
authors.affiliation: Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan.
authors.forename: Jian-Ren
authors.initials: JR
authors.lastname: Shen
mesh_terms: D020134:Catalytic Domain; D003460:Crystallization; D000458:Cyanobacteria / Q000201:enzymology*; D004583:Electrons; D007834:Lasers; D008345:Manganese / Q000737:chemistry; D008958:Models, Molecular; D010100:Oxygen / Q000737:chemistry / Q000378:metabolism; D045332:Photosystem II Protein Complex / Q000737:chemistry* / Q000528:radiation effects*; D017356:Synchrotrons; D013997:Time Factors; D014867:Water / Q000737:chemistry / Q000378:metabolism; D014965:X-Rays
chemical_list: D045332:Photosystem II Protein Complex; D014867:Water; D008345:Manganese; D010100:Oxygen