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Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å

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  • Yasufumi Umena

    (Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi
    Present addresses: Institute for Protein Research, Osaka University, Suita, Osaka 565-0871, Japan (Y.U.); Department of Chemistry, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (K.K.); The OCU Advanced Research Institute for Natural Science and Technology (OCARINA), Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (N.K.).)

  • Keisuke Kawakami

    (Graduate School of Natural Science and Technology/Faculty of Science
    Okayama University
    Present addresses: Institute for Protein Research, Osaka University, Suita, Osaka 565-0871, Japan (Y.U.); Department of Chemistry, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (K.K.); The OCU Advanced Research Institute for Natural Science and Technology (OCARINA), Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (N.K.).)

  • Jian-Ren Shen

    (Graduate School of Natural Science and Technology/Faculty of Science
    Okayama University)

  • Nobuo Kamiya

    (Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi
    Present addresses: Institute for Protein Research, Osaka University, Suita, Osaka 565-0871, Japan (Y.U.); Department of Chemistry, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (K.K.); The OCU Advanced Research Institute for Natural Science and Technology (OCARINA), Osaka City University, 3-3-138 Sugimoto, Sumiyoshi, Osaka 558-8585, Japan (N.K.).)

Abstract

Photosystem II is the site of photosynthetic water oxidation and contains 20 subunits with a total molecular mass of 350 kDa. The structure of photosystem II has been reported at resolutions from 3.8 to 2.9 Å. These resolutions have provided much information on the arrangement of protein subunits and cofactors but are insufficient to reveal the detailed structure of the catalytic centre of water splitting. Here we report the crystal structure of photosystem II at a resolution of 1.9 Å. From our electron density map, we located all of the metal atoms of the Mn4CaO5 cluster, together with all of their ligands. We found that five oxygen atoms served as oxo bridges linking the five metal atoms, and that four water molecules were bound to the Mn4CaO5 cluster; some of them may therefore serve as substrates for dioxygen formation. We identified more than 1,300 water molecules in each photosystem II monomer. Some of them formed extensive hydrogen-bonding networks that may serve as channels for protons, water or oxygen molecules. The determination of the high-resolution structure of photosystem II will allow us to analyse and understand its functions in great detail.

Suggested Citation

  • Yasufumi Umena & Keisuke Kawakami & Jian-Ren Shen & Nobuo Kamiya, 2011. "Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å," Nature, Nature, vol. 473(7345), pages 55-60, May.
    • Handle: RePEc:nat:nature:v:473:y:2011:i:7345:d:10.1038_nature09913
    DOI: 10.1038/nature09913
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    1. Yusuke Yoneda & Eric A. Arsenault & Shiun-Jr Yang & Kaydren Orcutt & Masakazu Iwai & Graham R. Fleming, 2022. "The initial charge separation step in oxygenic photosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Zhiyuan Mao & Xingyue Li & Zhenhua Li & Liangliang Shen & Xiaoyi Li & Yanyan Yang & Wenda Wang & Tingyun Kuang & Jian-Ren Shen & Guangye Han, 2024. "Structure and distinct supramolecular organization of a PSII-ACPII dimer from a cryptophyte alga Chroomonas placoidea," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Rana Hussein & Mohamed Ibrahim & Asmit Bhowmick & Philipp S. Simon & Ruchira Chatterjee & Louise Lassalle & Margaret Doyle & Isabel Bogacz & In-Sik Kim & Mun Hon Cheah & Sheraz Gul & Casper Lichtenber, 2021. "Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Ryo Nagao & Koji Kato & Tasuku Hamaguchi & Yoshifumi Ueno & Naoki Tsuboshita & Shota Shimizu & Miyu Furutani & Shigeki Ehira & Yoshiki Nakajima & Keisuke Kawakami & Takehiro Suzuki & Naoshi Dohmae & S, 2023. "Structure of a monomeric photosystem I core associated with iron-stress-induced-A proteins from Anabaena sp. PCC 7120," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Lin Zhang & Junxiang Ruan & Fudan Gao & Qiang Xin & Li-Ping Che & Lujuan Cai & Zekun Liu & Mengmeng Kong & Jean-David Rochaix & Hualing Mi & Lianwei Peng, 2024. "Thylakoid protein FPB1 synergistically cooperates with PAM68 to promote CP47 biogenesis and Photosystem II assembly," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Shangkun Li & Zeyi Zhang & Walker R. Marks & Xinan Huang & Hang Chen & Dragos C. Stoian & Rolf Erni & Carlos A. Triana & Greta R. Patzke, 2024. "{Co4O4} Cubanes in a conducting polymer matrix as bio-inspired molecular oxygen evolution catalysts," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Ryan Puskar & Chloe Truong & Kyle Swain & Saborni Chowdhury & Ka-Yi Chan & Shan Li & Kai-Wen Cheng & Ting Yu Wang & Yu-Ping Poh & Yuval Mazor & Haijun Liu & Tsui-Fen Chou & Brent L. Nannenga & Po-Lin , 2022. "Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    8. Ziyu Zhao & Irene Vercellino & Jana Knoppová & Roman Sobotka & James W. Murray & Peter J. Nixon & Leonid A. Sazanov & Josef Komenda, 2023. "The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    9. Xiaojing Lin & Zhaojie Wang & Shoufu Cao & Yuying Hu & Siyuan Liu & Xiaodong Chen & Hongyu Chen & Xingheng Zhang & Shuxian Wei & Hui Xu & Zhi Cheng & Qi Hou & Daofeng Sun & Xiaoqing Lu, 2023. "Bioinspired trimesic acid anchored electrocatalysts with unique static and dynamic compatibility for enhanced water oxidation," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    10. Shishang Dong & Guoqiang Huang & Changhui Wang & Jiajia Wang & Sen-Fang Sui & Xiaochun Qin, 2022. "Structure of the Acidobacteria homodimeric reaction center bound with cytochrome c," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Vincenzo Mascoli & Ahmad Farhan Bhatti & Luca Bersanini & Herbert Amerongen & Roberta Croce, 2022. "The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    12. Ganesh, Ibram, 2015. "Solar fuels vis-à-vis electricity generation from sunlight: The current state-of-the-art (a review)," Renewable and Sustainable Energy Reviews, Elsevier, vol. 44(C), pages 904-932.
    13. Koji Kato & Ryo Nagao & Yoshifumi Ueno & Makio Yokono & Takehiro Suzuki & Tian-Yi Jiang & Naoshi Dohmae & Fusamichi Akita & Seiji Akimoto & Naoyuki Miyazaki & Jian-Ren Shen, 2022. "Structure of a tetrameric photosystem I from a glaucophyte alga Cyanophora paradoxa," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Joseph T Snow & Despo Polyviou & Paul Skipp & Nathan A M Chrismas & Andrew Hitchcock & Richard Geider & C Mark Moore & Thomas S Bibby, 2015. "Quantifying Integrated Proteomic Responses to Iron Stress in the Globally Important Marine Diazotroph Trichodesmium," PLOS ONE, Public Library of Science, vol. 10(11), pages 1-24, November.
    15. Xuelei Pan & Mengyu Yan & Qian Liu & Xunbiao Zhou & Xiaobin Liao & Congli Sun & Jiexin Zhu & Callum McAleese & Pierre Couture & Matthew K. Sharpe & Richard Smith & Nianhua Peng & Jonathan England & Sh, 2024. "Electric-field-assisted proton coupling enhanced oxygen evolution reaction," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    16. Futing Zhang & Zuozhu Wen & Shanlin Wang & Weiyi Tang & Ya-Wei Luo & Sven A. Kranz & Haizheng Hong & Dalin Shi, 2022. "Phosphate limitation intensifies negative effects of ocean acidification on globally important nitrogen fixing cyanobacterium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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