Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses

Michihiro Suga, Fusamichi Akita, Kunio Hirata, Go Ueno, Hironori Murakami, Yoshiki Nakajima, Tetsuya Shimizu, Keitaro Yamashita, Masaki Yamamoto, Hideo Ago, Jian-Ren Shen

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Abstract

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.

Original languageEnglish
Pages (from-to)99-103
Number of pages5
JournalNature
Volume517
Issue number7532
DOIs
Publication statusPublished - Jan 1 2015

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Photosystem II Protein Complex
X-Rays
Oxygen
Photosynthesis
Manganese
X-Ray Diffraction
Lasers
Electrons
Water
Cations
Membrane Proteins
Radiation
Ligands
Light

ASJC Scopus subject areas

  • General
  • Medicine(all)

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Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses. / Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio; Ueno, Go; Murakami, Hironori; Nakajima, Yoshiki; Shimizu, Tetsuya; Yamashita, Keitaro; Yamamoto, Masaki; Ago, Hideo; Shen, Jian-Ren.

In: Nature, Vol. 517, No. 7532, 01.01.2015, p. 99-103.

Research output: Contribution to journalArticle

Suga, M, Akita, F, Hirata, K, Ueno, G, Murakami, H, Nakajima, Y, Shimizu, T, Yamashita, K, Yamamoto, M, Ago, H & Shen, J-R 2015, 'Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses', Nature, vol. 517, no. 7532, pp. 99-103. https://doi.org/10.1038/nature13991
Suga, Michihiro ; Akita, Fusamichi ; Hirata, Kunio ; Ueno, Go ; Murakami, Hironori ; Nakajima, Yoshiki ; Shimizu, Tetsuya ; Yamashita, Keitaro ; Yamamoto, Masaki ; Ago, Hideo ; Shen, Jian-Ren. / Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses. In: Nature. 2015 ; Vol. 517, No. 7532. pp. 99-103.
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abstract = "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°ngstr{\"o}mresolution, 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°ngstr{\"o}ms using femtosecond X-ray pulses of the SPring-8 {\aa}ngstr{\"o}mcompact 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°ngstr{\"o}ms. 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.",
author = "Michihiro Suga and Fusamichi Akita and Kunio Hirata and Go Ueno and Hironori Murakami and Yoshiki Nakajima and Tetsuya Shimizu and Keitaro Yamashita and Masaki Yamamoto and Hideo Ago and Jian-Ren Shen",
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AU - Murakami, Hironori

AU - Nakajima, Yoshiki

AU - Shimizu, Tetsuya

AU - Yamashita, Keitaro

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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.

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