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

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

Journal

• Nature

  Nature 543 (7643), 131-135, 2017-03

  Nature Publishing Group

Keywords

• Multidisciplinary

Details

• CRID: 1050283687312856832
• NII Article ID: 120006344935
• NII Book ID: AA00752384
• ISSN: 00280836
• ISSN: 14764687
• DOI: 10.1038/nature21400
• Web Site: https://ousar.lib.okayama-u.ac.jp/55218
• Web Site: http://www.nature.com/articles/nature21400.pdf
• Web Site: http://www.nature.com/articles/nature21400
• Text Lang: en
• Article Type: journal article
• Data Source:
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