Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

Michihiro Suga, Fusamichi Akita, Michihiro Sugahara, Minoru Kubo, Yoshiki Nakajima, Takanori Nakane, Keitaro Yamashita, Yasufumi Umena, Makoto Nakabayashi, Takahiro Yamane, Takamitsu Nakano, Mamoru Suzuki, Tetsuya Masuda, Shigeyuki Inoue, Tetsunari Kimura, Takashi Nomura, Shinichiro Yonekura, Long-Jiang Yu, Tomohiro Sakamoto, Taiki MotomuraJing-Hua Chen, Yuki Kato, Takumi Noguchi, Kensuke Tono, Yasumasa Joti, Takashi Kameshima, Takaki Hatsui, Eriko Nango, Rie Tanaka, Hisashi Naitow, Yoshinori Matsuura, Ayumi Yamashita, Masaki Yamamoto, Osamu Nureki, Makina Yabashi, Tetsuya Ishikawa, So Iwata, Jian-Ren Shen

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Abstract

Photosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer. It catalyses light-driven water oxidation at its catalytic centre, the oxygen-evolving complex (OEC). The structure of PSII has been analysed at 1.9 Å resolution by synchrotron radiation X-rays, which revealed that the OEC is a Mn4CaO5 cluster organized in an asymmetric, 'distorted-chair' form. This structure was further analysed with femtosecond X-ray free electron lasers (XFEL), providing the 'radiation damage-free' structure. The mechanism of O=O bond formation, however, remains obscure owing to the lack of intermediate-state structures. Here we describe the structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 Å using time-resolved serial femtosecond crystallography with an XFEL provided by the SPring-8 ångström compact free-electron laser. An isomorphous difference Fourier map between the two-flash and dark-adapted states revealed two areas of apparent changes: around the QB/non-haem iron and the Mn4CaO5 cluster. The changes around the QB/non-haem iron region reflected the electron and proton transfers induced by the two-flash illumination. In the region around the OEC, a water molecule located 3.5 Å from the Mn4CaO5 cluster disappeared from the map upon two-flash illumination. This reduced the distance between another water molecule and the oxygen atom O4, suggesting that proton transfer also occurred. Importantly, the two-flash-minus-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ4-oxo-bridge located in the quasi-centre of Mn1 and Mn4 (refs 4,5). This suggests the insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 Å between these two oxygen atoms. This provides a mechanism for the O=O bond formation consistent with that proposed previously.

Original languageEnglish
JournalNature
DOIs
Publication statusE-pub ahead of print - Feb 20 2017

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Photosystem II Protein Complex
Lasers
X-Rays
Electrons
Oxygen
Light
Lighting
Protons
Water
Iron
Radiation
Synchrotrons
X Ray Crystallography
Membrane Proteins
Temperature

Keywords

  • Journal Article

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Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. / Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro; Kubo, Minoru; Nakajima, Yoshiki; Nakane, Takanori; Yamashita, Keitaro; Umena, Yasufumi; Nakabayashi, Makoto; Yamane, Takahiro; Nakano, Takamitsu; Suzuki, Mamoru; Masuda, Tetsuya; Inoue, Shigeyuki; Kimura, Tetsunari; Nomura, Takashi; Yonekura, Shinichiro; Yu, Long-Jiang; Sakamoto, Tomohiro; Motomura, Taiki; Chen, Jing-Hua; Kato, Yuki; Noguchi, Takumi; Tono, Kensuke; Joti, Yasumasa; Kameshima, Takashi; Hatsui, Takaki; Nango, Eriko; Tanaka, Rie; Naitow, Hisashi; Matsuura, Yoshinori; Yamashita, Ayumi; Yamamoto, Masaki; Nureki, Osamu; Yabashi, Makina; Ishikawa, Tetsuya; Iwata, So; Shen, Jian-Ren.

In: Nature, 20.02.2017.

Research output: Contribution to journalArticle

Suga, M, Akita, F, Sugahara, M, Kubo, M, Nakajima, Y, Nakane, T, Yamashita, K, Umena, Y, Nakabayashi, M, Yamane, T, Nakano, T, Suzuki, M, Masuda, T, Inoue, S, Kimura, T, Nomura, T, Yonekura, S, Yu, L-J, Sakamoto, T, Motomura, T, Chen, J-H, Kato, Y, Noguchi, T, Tono, K, Joti, Y, Kameshima, T, Hatsui, T, Nango, E, Tanaka, R, Naitow, H, Matsuura, Y, Yamashita, A, Yamamoto, M, Nureki, O, Yabashi, M, Ishikawa, T, Iwata, S & Shen, J-R 2017, 'Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL', Nature. https://doi.org/10.1038/nature21400
Suga, Michihiro ; Akita, Fusamichi ; Sugahara, Michihiro ; Kubo, Minoru ; Nakajima, Yoshiki ; Nakane, Takanori ; Yamashita, Keitaro ; Umena, Yasufumi ; Nakabayashi, Makoto ; Yamane, Takahiro ; Nakano, Takamitsu ; Suzuki, Mamoru ; Masuda, Tetsuya ; Inoue, Shigeyuki ; Kimura, Tetsunari ; Nomura, Takashi ; Yonekura, Shinichiro ; Yu, Long-Jiang ; Sakamoto, Tomohiro ; Motomura, Taiki ; Chen, Jing-Hua ; Kato, Yuki ; Noguchi, Takumi ; Tono, Kensuke ; Joti, Yasumasa ; Kameshima, Takashi ; Hatsui, Takaki ; Nango, Eriko ; Tanaka, Rie ; Naitow, Hisashi ; Matsuura, Yoshinori ; Yamashita, Ayumi ; Yamamoto, Masaki ; Nureki, Osamu ; Yabashi, Makina ; Ishikawa, Tetsuya ; Iwata, So ; Shen, Jian-Ren. / Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. In: Nature. 2017.
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title = "Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL",
abstract = "Photosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer. It catalyses light-driven water oxidation at its catalytic centre, the oxygen-evolving complex (OEC). The structure of PSII has been analysed at 1.9 {\AA} resolution by synchrotron radiation X-rays, which revealed that the OEC is a Mn4CaO5 cluster organized in an asymmetric, 'distorted-chair' form. This structure was further analysed with femtosecond X-ray free electron lasers (XFEL), providing the 'radiation damage-free' structure. The mechanism of O=O bond formation, however, remains obscure owing to the lack of intermediate-state structures. Here we describe the structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 {\AA} using time-resolved serial femtosecond crystallography with an XFEL provided by the SPring-8 {\aa}ngstr{\"o}m compact free-electron laser. An isomorphous difference Fourier map between the two-flash and dark-adapted states revealed two areas of apparent changes: around the QB/non-haem iron and the Mn4CaO5 cluster. The changes around the QB/non-haem iron region reflected the electron and proton transfers induced by the two-flash illumination. In the region around the OEC, a water molecule located 3.5 {\AA} from the Mn4CaO5 cluster disappeared from the map upon two-flash illumination. This reduced the distance between another water molecule and the oxygen atom O4, suggesting that proton transfer also occurred. Importantly, the two-flash-minus-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ4-oxo-bridge located in the quasi-centre of Mn1 and Mn4 (refs 4,5). This suggests the insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 {\AA} between these two oxygen atoms. This provides a mechanism for the O=O bond formation consistent with that proposed previously.",
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author = "Michihiro Suga and Fusamichi Akita and Michihiro Sugahara and Minoru Kubo and Yoshiki Nakajima and Takanori Nakane and Keitaro Yamashita and Yasufumi Umena and Makoto Nakabayashi and Takahiro Yamane and Takamitsu Nakano and Mamoru Suzuki and Tetsuya Masuda and Shigeyuki Inoue and Tetsunari Kimura and Takashi Nomura and Shinichiro Yonekura and Long-Jiang Yu and Tomohiro Sakamoto and Taiki Motomura and Jing-Hua Chen and Yuki Kato and Takumi Noguchi and Kensuke Tono and Yasumasa Joti and Takashi Kameshima and Takaki Hatsui and Eriko Nango and Rie Tanaka and Hisashi Naitow and Yoshinori Matsuura and Ayumi Yamashita and Masaki Yamamoto and Osamu Nureki and Makina Yabashi and Tetsuya Ishikawa and So Iwata and Jian-Ren Shen",
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T1 - Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

AU - Suga, Michihiro

AU - Akita, Fusamichi

AU - Sugahara, Michihiro

AU - Kubo, Minoru

AU - Nakajima, Yoshiki

AU - Nakane, Takanori

AU - Yamashita, Keitaro

AU - Umena, Yasufumi

AU - Nakabayashi, Makoto

AU - Yamane, Takahiro

AU - Nakano, Takamitsu

AU - Suzuki, Mamoru

AU - Masuda, Tetsuya

AU - Inoue, Shigeyuki

AU - Kimura, Tetsunari

AU - Nomura, Takashi

AU - Yonekura, Shinichiro

AU - Yu, Long-Jiang

AU - Sakamoto, Tomohiro

AU - Motomura, Taiki

AU - Chen, Jing-Hua

AU - Kato, Yuki

AU - Noguchi, Takumi

AU - Tono, Kensuke

AU - Joti, Yasumasa

AU - Kameshima, Takashi

AU - Hatsui, Takaki

AU - Nango, Eriko

AU - Tanaka, Rie

AU - Naitow, Hisashi

AU - Matsuura, Yoshinori

AU - Yamashita, Ayumi

AU - Yamamoto, Masaki

AU - Nureki, Osamu

AU - Yabashi, Makina

AU - Ishikawa, Tetsuya

AU - Iwata, So

AU - Shen, Jian-Ren

PY - 2017/2/20

Y1 - 2017/2/20

N2 - Photosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer. It catalyses light-driven water oxidation at its catalytic centre, the oxygen-evolving complex (OEC). The structure of PSII has been analysed at 1.9 Å resolution by synchrotron radiation X-rays, which revealed that the OEC is a Mn4CaO5 cluster organized in an asymmetric, 'distorted-chair' form. This structure was further analysed with femtosecond X-ray free electron lasers (XFEL), providing the 'radiation damage-free' structure. The mechanism of O=O bond formation, however, remains obscure owing to the lack of intermediate-state structures. Here we describe the structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 Å using time-resolved serial femtosecond crystallography with an XFEL provided by the SPring-8 ångström compact free-electron laser. An isomorphous difference Fourier map between the two-flash and dark-adapted states revealed two areas of apparent changes: around the QB/non-haem iron and the Mn4CaO5 cluster. The changes around the QB/non-haem iron region reflected the electron and proton transfers induced by the two-flash illumination. In the region around the OEC, a water molecule located 3.5 Å from the Mn4CaO5 cluster disappeared from the map upon two-flash illumination. This reduced the distance between another water molecule and the oxygen atom O4, suggesting that proton transfer also occurred. Importantly, the two-flash-minus-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ4-oxo-bridge located in the quasi-centre of Mn1 and Mn4 (refs 4,5). This suggests the insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 Å between these two oxygen atoms. This provides a mechanism for the O=O bond formation consistent with that proposed previously.

AB - Photosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer. It catalyses light-driven water oxidation at its catalytic centre, the oxygen-evolving complex (OEC). The structure of PSII has been analysed at 1.9 Å resolution by synchrotron radiation X-rays, which revealed that the OEC is a Mn4CaO5 cluster organized in an asymmetric, 'distorted-chair' form. This structure was further analysed with femtosecond X-ray free electron lasers (XFEL), providing the 'radiation damage-free' structure. The mechanism of O=O bond formation, however, remains obscure owing to the lack of intermediate-state structures. Here we describe the structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 Å using time-resolved serial femtosecond crystallography with an XFEL provided by the SPring-8 ångström compact free-electron laser. An isomorphous difference Fourier map between the two-flash and dark-adapted states revealed two areas of apparent changes: around the QB/non-haem iron and the Mn4CaO5 cluster. The changes around the QB/non-haem iron region reflected the electron and proton transfers induced by the two-flash illumination. In the region around the OEC, a water molecule located 3.5 Å from the Mn4CaO5 cluster disappeared from the map upon two-flash illumination. This reduced the distance between another water molecule and the oxygen atom O4, suggesting that proton transfer also occurred. Importantly, the two-flash-minus-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ4-oxo-bridge located in the quasi-centre of Mn1 and Mn4 (refs 4,5). This suggests the insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 Å between these two oxygen atoms. This provides a mechanism for the O=O bond formation consistent with that proposed previously.

KW - Journal Article

U2 - 10.1038/nature21400

DO - 10.1038/nature21400

M3 - Article

C2 - 28219079

JO - Nature

JF - Nature

SN - 0028-0836

ER -