TY - JOUR
T1 - Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses
AU - Suga, Michihiro
AU - Akita, Fusamichi
AU - Hirata, Kunio
AU - Ueno, Go
AU - Murakami, Hironori
AU - Nakajima, Yoshiki
AU - Shimizu, Tetsuya
AU - Yamashita, Keitaro
AU - Yamamoto, Masaki
AU - Ago, Hideo
AU - Shen, Jian Ren
N1 - Publisher Copyright:
© 2015 Macmillan Publishers Limited. All rights reserved.
PY - 2015/1/1
Y1 - 2015/1/1
N2 - Photosynthesis converts light energy into biologically useful chemical energy vital to life onEarth.The initial reactionof 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 a°ngströmresolution, which revealed that theOEC is aMn4CaO5-cluster coordinated by a well defined protein environment1. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation2, and slight differences were found in the Mn-Mn distances determined by XRD1, EXAFS3-7 and theoretical studies8-14.Herewe report a 'radiation-damage-free' structure ofPSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 a°ngströms using femtosecond X-ray pulses of the SPring-8 ångströmcompact free-electron laser (SACLA) and hundreds of large, highly isomorphousPSII 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 a°ngströms. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) andMn4A(III), based on the averageMn-ligand distances and analysis of the Jahn-Teller axis on Mn(III). One of the oxobridged 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 oneof 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.
AB - Photosynthesis converts light energy into biologically useful chemical energy vital to life onEarth.The initial reactionof 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 a°ngströmresolution, which revealed that theOEC is aMn4CaO5-cluster coordinated by a well defined protein environment1. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation2, and slight differences were found in the Mn-Mn distances determined by XRD1, EXAFS3-7 and theoretical studies8-14.Herewe report a 'radiation-damage-free' structure ofPSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 a°ngströms using femtosecond X-ray pulses of the SPring-8 ångströmcompact free-electron laser (SACLA) and hundreds of large, highly isomorphousPSII 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 a°ngströms. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) andMn4A(III), based on the averageMn-ligand distances and analysis of the Jahn-Teller axis on Mn(III). One of the oxobridged 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 oneof 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.
UR - http://www.scopus.com/inward/record.url?scp=84921499454&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84921499454&partnerID=8YFLogxK
U2 - 10.1038/nature13991
DO - 10.1038/nature13991
M3 - Article
C2 - 25470056
AN - SCOPUS:84921499454
VL - 517
SP - 99
EP - 103
JO - Nature
JF - Nature
SN - 0028-0836
IS - 7532
ER -