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Cryo-EM Structure of the Photosynthetic LH1-RC Complex from Rhodospirillum rubrum

  • Kazutoshi Tani*
    Kazutoshi Tani
    Graduate School of Medicine, Mie University, Tsu, Mie 514-8507, Japan
    *Email: [email protected]
  • Ryo Kanno
    Ryo Kanno
    Imaging Section, Research Support Division, Okinawa Institute of Science and Technology Graduate University (OIST), 1919-1, Tancha, Onna-son, Kunigami-gun, Okinawa 904-0495, Japan
    More by Ryo Kanno
  • Xuan-Cheng Ji
    Xuan-Cheng Ji
    Faculty of Science, Ibaraki University, Mito, Ibaraki 310-8512, Japan
  • Malgorzata Hall
    Malgorzata Hall
    Imaging Section, Research Support Division, Okinawa Institute of Science and Technology Graduate University (OIST), 1919-1, Tancha, Onna-son, Kunigami-gun, Okinawa 904-0495, Japan
  • Long-Jiang Yu
    Long-Jiang Yu
    Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
  • Yukihiro Kimura
    Yukihiro Kimura
    Department of Agrobioscience, Graduate School of Agriculture, Kobe University, Nada, Kobe, Hyogo 657-8501, Japan
  • Michael T. Madigan
    Michael T. Madigan
    School of Biological Sciences, Southern Illinois University, Carbondale, Illinois 62901, United States
  • Akira Mizoguchi
    Akira Mizoguchi
    Graduate School of Medicine, Mie University, Tsu, Mie 514-8507, Japan
  • Bruno M. Humbel
    Bruno M. Humbel
    Imaging Section, Research Support Division, Okinawa Institute of Science and Technology Graduate University (OIST), 1919-1, Tancha, Onna-son, Kunigami-gun, Okinawa 904-0495, Japan
  • , and 
  • Zheng-Yu Wang-Otomo*
    Zheng-Yu Wang-Otomo
    Faculty of Science, Ibaraki University, Mito, Ibaraki 310-8512, Japan
    *Email: [email protected]
Cite this: Biochemistry 2021, 60, 32, 2483–2491
Publication Date (Web):July 29, 2021
https://doi.org/10.1021/acs.biochem.1c00360
Copyright © 2021 American Chemical Society

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    Abstract

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    Rhodospirillum (Rsp.) rubrum is one of the most widely used model organisms in bacterial photosynthesis. This purple phototroph is characterized by the presence of both rhodoquinone (RQ) and ubiquinone as electron carriers and bacteriochlorophyll (BChl) a esterified at the propionic acid side chain by geranylgeraniol (BChl aG) instead of phytol. Despite intensive efforts, the structure of the light-harvesting-reaction center (LH1-RC) core complex from Rsp. rubrum remains at low resolutions. Using cryo-EM, here we present a robust new view of the Rsp. rubrum LH1-RC at 2.76 Å resolution. The LH1 complex forms a closed, slightly elliptical ring structure with 16 αβ-polypeptides surrounding the RC. Our biochemical analysis detected RQ molecules in the purified LH1-RC, and the cryo-EM density map specifically positions RQ at the QA site in the RC. The geranylgeraniol side chains of BChl aG coordinated by LH1 β-polypeptides exhibit a highly homologous tail-up conformation that allows for interactions with the bacteriochlorin rings of nearby LH1 α-associated BChls aG. The structure also revealed key protein–protein interactions in both N- and C-terminal regions of the LH1 αβ-polypeptides, mainly within a face-to-face structural subunit. Our high-resolution Rsp. rubrum LH1-RC structure provides new insight for evaluating past experimental and computational results obtained with this old organism over many decades and lays the foundation for more detailed exploration of light-energy conversion, quinone transport, and structure–function relationships in this pigment–protein complex.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.biochem.1c00360.

    • Cryo-EM data statistics; comparison of distances for His-BChl(Mg) and BChl(Mg)-BChl(Mg); absorption, CD and MCD spectra of the purified LH1-RC; electron micrographs; biochemical analyses of the quinones; cryo-EM structure determination; sequence information on LH1 polypeptides; structural comparison with NMR solution structures; conformations of LH1 BChl a esterified by phytyl group; sequence comparison of RC subunits; key residues around RC special pair; conserved Tyr residue near the RC special pair; a back-to-back subunit of LH1 complex (PDF)

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    The map and model have been deposited in the EMDB and PDB with the following accession codes: 31258 and 7EQD. All other data and materials are available from the authors upon reasonable request.

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    Cited By

    This article is cited by 12 publications.

    1. Yukihiro Kimura, Kazutoshi Tani, Michael T. Madigan, Zheng-Yu Wang-Otomo. Advances in the Spectroscopic and Structural Characterization of Core Light-Harvesting Complexes from Purple Phototrophic Bacteria. The Journal of Physical Chemistry B 2023, 127 (1) , 6-17. https://doi.org/10.1021/acs.jpcb.2c06638
    2. Laura Bracun, Atsushi Yamagata, Bern M. Christianson, Mikako Shirouzu, Lu-Ning Liu. Cryo-EM structure of a monomeric RC-LH1-PufX supercomplex with high-carotenoid content from Rhodobacter capsulatus. Structure 2023, 31 (3) , 318-328.e3. https://doi.org/10.1016/j.str.2023.01.006
    3. Peng Cao, Laura Bracun, Atsushi Yamagata, Bern M. Christianson, Tatsuki Negami, Baohua Zou, Tohru Terada, Daniel P. Canniffe, Mikako Shirouzu, Mei Li, Lu-Ning Liu. Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-29563-3
    4. Kazutoshi Tani, Ryo Kanno, Keigo Kurosawa, Shinichi Takaichi, Kenji V. P. Nagashima, Malgorzata Hall, Long-Jiang Yu, Yukihiro Kimura, Michael T. Madigan, Akira Mizoguchi, Bruno M. Humbel, Zheng-Yu Wang-Otomo. An LH1–RC photocomplex from an extremophilic phototroph provides insight into origins of two photosynthesis proteins. Communications Biology 2022, 5 (1) https://doi.org/10.1038/s42003-022-04174-2
    5. Nao Yukihira, Chiasa Uragami, Kota Horiuchi, Daisuke Kosumi, Alastair T. Gardiner, Richard J. Cogdell, Hideki Hashimoto. Intramolecular charge-transfer enhances energy transfer efficiency in carotenoid-reconstituted light-harvesting 1 complex of purple photosynthetic bacteria. Communications Chemistry 2022, 5 (1) https://doi.org/10.1038/s42004-022-00749-6
    6. Mitsuaki Hirose, Yusuke Tsukatani, Jiro Harada, Hitoshi Tamiaki. Characterization of regioisomeric diterpenoid tails in bacteriochlorophylls produced by geranylgeranyl reductase from Halorhodospira halochloris and Blastochloris viridis. Photosynthesis Research 2022, 154 (1) , 1-12. https://doi.org/10.1007/s11120-022-00938-3
    7. Yukihiro Kimura, Michie Imanishi, Yong Li, Yuki Yura, Takashi Ohno, Yoshitaka Saga, Michael T. Madigan, Zheng-Yu Wang-Otomo. Identification of metal-sensitive structural changes in the Ca 2+ -binding photocomplex from Thermochromatium tepidum by isotope-edited vibrational spectroscopy. The Journal of Chemical Physics 2022, 156 (10) , 105101. https://doi.org/10.1063/5.0075600
    8. George A. Sutherland, Pu Qian, C. Neil Hunter, David J.K. Swainsbury, Andrew Hitchcock. Engineering purple bacterial carotenoid biosynthesis to study the roles of carotenoids in light-harvesting complexes. 2022, 137-184. https://doi.org/10.1016/bs.mie.2022.04.001
    9. Toru Kondo, Yutaka Shibata. Recent advances in single-molecule spectroscopy studies on light-harvesting processes in oxygenic photosynthesis. Biophysics and Physicobiology 2022, 19 (0) , n/a. https://doi.org/10.2142/biophysico.bppb-v19.0013
    10. Kazutoshi Tani, Kenji V. P. Nagashima, Ryo Kanno, Saki Kawamura, Riku Kikuchi, Malgorzata Hall, Long-Jiang Yu, Yukihiro Kimura, Michael T. Madigan, Akira Mizoguchi, Bruno M. Humbel, Zheng-Yu Wang-Otomo. A previously unrecognized membrane protein in the Rhodobacter sphaeroides LH1-RC photocomplex. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-021-26561-9
    11. Pu Qian, Tristan I. Croll, Andrew Hitchcock, Philip J. Jackson, Jack H. Salisbury, Pablo Castro-Hartmann, Kasim Sader, David J.K. Swainsbury, C. Neil Hunter. Cryo-EM structure of the dimeric Rhodobacter sphaeroides RC-LH1 core complex at 2.9 Å: the structural basis for dimerisation. Biochemical Journal 2021, 478 (21) , 3923-3937. https://doi.org/10.1042/BCJ20210696
    12. Pu Qian, David J.K. Swainsbury, Tristan I. Croll, Jack H. Salisbury, Elizabeth C. Martin, Philip J. Jackson, Andrew Hitchcock, Pablo Castro-Hartmann, Kasim Sader, C. Neil Hunter. Cryo-EM structure of the monomeric Rhodobacter sphaeroides RC–LH1 core complex at 2.5 Å. Biochemical Journal 2021, 478 (20) , 3775-3790. https://doi.org/10.1042/BCJ20210631

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