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Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex

Author

Listed:
  • Peng Cao

    (Chinese Academy of Sciences
    Faculty of Environment and Life, Beijing University of Technology)

  • Laura Bracun

    (University of Liverpool
    Laboratory for Protein Functional and Structural Biology, RIKEN Center for Biosystems Dynamics Research)

  • Atsushi Yamagata

    (Laboratory for Protein Functional and Structural Biology, RIKEN Center for Biosystems Dynamics Research)

  • Bern M. Christianson

    (University of Liverpool)

  • Tatsuki Negami

    (Graduate School of Agricultural and Life Sciences, University of Tokyo)

  • Baohua Zou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Tohru Terada

    (Graduate School of Agricultural and Life Sciences, University of Tokyo)

  • Daniel P. Canniffe

    (University of Liverpool)

  • Mikako Shirouzu

    (Laboratory for Protein Functional and Structural Biology, RIKEN Center for Biosystems Dynamics Research)

  • Mei Li

    (Chinese Academy of Sciences)

  • Lu-Ning Liu

    (University of Liverpool
    College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China)

Abstract

The reaction center (RC) and light-harvesting complex 1 (LH1) form a RC–LH1 core supercomplex that is vital for the primary reactions of photosynthesis in purple phototrophic bacteria. Some species possess the dimeric RC–LH1 complex with a transmembrane polypeptide PufX, representing the largest photosynthetic complex in anoxygenic phototrophs. However, the details of the architecture and assembly mechanism of the RC–LH1 dimer are unclear. Here we report seven cryo-electron microscopy (cryo-EM) structures of RC–LH1 supercomplexes from Rhodobacter sphaeroides. Our structures reveal that two PufX polypeptides are positioned in the center of the S-shaped RC–LH1 dimer, interlocking association between the components and mediating RC–LH1 dimerization. Moreover, we identify another transmembrane peptide, designated PufY, which is located between the RC and LH1 subunits near the LH1 opening. PufY binds a quinone molecule and prevents LH1 subunits from completely encircling the RC, creating a channel for quinone/quinol exchange. Genetic mutagenesis, cryo-EM structures, and computational simulations provide a mechanistic understanding of the assembly and electron transport pathways of the RC–LH1 dimer and elucidate the roles of individual components in ensuring the structural and functional integrity of the photosynthetic supercomplex.

Suggested Citation

  • 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, 2022. "Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29563-3
    DOI: 10.1038/s41467-022-29563-3
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    References listed on IDEAS

    as
    1. Yueyong Xin & Yang Shi & Tongxin Niu & Qingqiang Wang & Wanqiang Niu & Xiaojun Huang & Wei Ding & Lei Yang & Robert E. Blankenship & Xiaoling Xu & Fei Sun, 2018. "Cryo-EM structure of the RC-LH core complex from an early branching photosynthetic prokaryote," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    2. Pu Qian & C. Alistair Siebert & Peiyi Wang & Daniel P. Canniffe & C. Neil Hunter, 2018. "Cryo-EM structure of the Blastochloris viridis LH1–RC complex at 2.9 Å," Nature, Nature, vol. 556(7700), pages 203-208, April.
    3. 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-Y, 2021. "A previously unrecognized membrane protein in the Rhodobacter sphaeroides LH1-RC photocomplex," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    4. Satomi Niwa & Long-Jiang Yu & Kazuki Takeda & Yu Hirano & Tomoaki Kawakami & Zheng-Yu Wang-Otomo & Kunio Miki, 2014. "Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å," Nature, Nature, vol. 508(7495), pages 228-232, April.
    5. Long-Jiang Yu & Michihiro Suga & Zheng-Yu Wang-Otomo & Jian-Ren Shen, 2018. "Structure of photosynthetic LH1–RC supercomplex at 1.9 Å resolution," Nature, Nature, vol. 556(7700), pages 209-213, April.
    6. Svetlana Bahatyrova & Raoul N. Frese & C. Alistair Siebert & John D. Olsen & Kees O. van der Werf & Rienk van Grondelle & Robert A. Niederman & Per A. Bullough & Cees Otto & C. Neil Hunter, 2004. "The native architecture of a photosynthetic membrane," Nature, Nature, vol. 430(7003), pages 1058-1062, August.
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