An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser

Michihiro Suga, Fusamichi Akita, Keitaro Yamashita, Yoshiki Nakajima, Go Ueno, Hongjie Li, Takahiro Yamane, Kunio Hirata, Yasufumi Umena, Shinichiro Yonekura, Long Jiang Yu, Hironori Murakami, Takashi Nomura, Tetsunari Kimura, Minoru Kubo, Seiki Baba, Takashi Kumasaka, Kensuke Tono, Makina Yabashi, Hiroshi IsobeKizashi Yamaguchi, Masaki Yamamoto, Hideo Ago, Jian Ren Shen

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Photosynthetic water oxidation is catalyzed by the Mn4CaO5 cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S0 to S4). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S1, S2, and S3 states by x-ray free-electron laser serial crystallography. No insertion of water was found in S2, but flipping of D1 Glu189 upon transition to S3 leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn4CaO6 cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reve cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation.

Original languageEnglish
Pages (from-to)334-338
Number of pages5
JournalScience
Volume366
Issue number6463
DOIs
Publication statusPublished - Oct 18 2019

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Photosystem II Protein Complex
Lasers
X-Rays
Electrons
Oxygen
Water
Aquaporins
Crystallography
Protons
Ligands

ASJC Scopus subject areas

  • General

Cite this

An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. / Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro; Nakajima, Yoshiki; Ueno, Go; Li, Hongjie; Yamane, Takahiro; Hirata, Kunio; Umena, Yasufumi; Yonekura, Shinichiro; Yu, Long Jiang; Murakami, Hironori; Nomura, Takashi; Kimura, Tetsunari; Kubo, Minoru; Baba, Seiki; Kumasaka, Takashi; Tono, Kensuke; Yabashi, Makina; Isobe, Hiroshi; Yamaguchi, Kizashi; Yamamoto, Masaki; Ago, Hideo; Shen, Jian Ren.

In: Science, Vol. 366, No. 6463, 18.10.2019, p. 334-338.

Research output: Contribution to journalArticle

Suga, M, Akita, F, Yamashita, K, Nakajima, Y, Ueno, G, Li, H, Yamane, T, Hirata, K, Umena, Y, Yonekura, S, Yu, LJ, Murakami, H, Nomura, T, Kimura, T, Kubo, M, Baba, S, Kumasaka, T, Tono, K, Yabashi, M, Isobe, H, Yamaguchi, K, Yamamoto, M, Ago, H & Shen, JR 2019, 'An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser', Science, vol. 366, no. 6463, pp. 334-338. https://doi.org/10.1126/science.aax6998
Suga, Michihiro ; Akita, Fusamichi ; Yamashita, Keitaro ; Nakajima, Yoshiki ; Ueno, Go ; Li, Hongjie ; Yamane, Takahiro ; Hirata, Kunio ; Umena, Yasufumi ; Yonekura, Shinichiro ; Yu, Long Jiang ; Murakami, Hironori ; Nomura, Takashi ; Kimura, Tetsunari ; Kubo, Minoru ; Baba, Seiki ; Kumasaka, Takashi ; Tono, Kensuke ; Yabashi, Makina ; Isobe, Hiroshi ; Yamaguchi, Kizashi ; Yamamoto, Masaki ; Ago, Hideo ; Shen, Jian Ren. / An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. In: Science. 2019 ; Vol. 366, No. 6463. pp. 334-338.
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AU - Ueno, Go

AU - Li, Hongjie

AU - Yamane, Takahiro

AU - Hirata, Kunio

AU - Umena, Yasufumi

AU - Yonekura, Shinichiro

AU - Yu, Long Jiang

AU - Murakami, Hironori

AU - Nomura, Takashi

AU - Kimura, Tetsunari

AU - Kubo, Minoru

AU - Baba, Seiki

AU - Kumasaka, Takashi

AU - Tono, Kensuke

AU - Yabashi, Makina

AU - Isobe, Hiroshi

AU - Yamaguchi, Kizashi

AU - Yamamoto, Masaki

AU - Ago, Hideo

AU - Shen, Jian Ren

PY - 2019/10/18

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AB - Photosynthetic water oxidation is catalyzed by the Mn4CaO5 cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S0 to S4). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S1, S2, and S3 states by x-ray free-electron laser serial crystallography. No insertion of water was found in S2, but flipping of D1 Glu189 upon transition to S3 leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn4CaO6 cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reve cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation.

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