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Energetic robustness to large scale structural fluctuations in a photosynthetic supercomplex

Author

Listed:
  • Dvir Harris

    (Massachusetts Institute of Technology)

  • Hila Toporik

    (Arizona State University
    Arizona State University
    The Hebrew University of Jerusalem)

  • Gabriela S. Schlau-Cohen

    (Massachusetts Institute of Technology)

  • Yuval Mazor

    (Arizona State University
    Arizona State University)

Abstract

Photosynthetic organisms transport and convert solar energy with near-unity quantum efficiency using large protein supercomplexes held in flexible membranes. The individual proteins position chlorophylls to tight tolerances considered critical for fast and efficient energy transfer. The variability in protein organization within the supercomplexes, and how efficiency is maintained despite variability, had been unresolved. Here, we report on structural heterogeneity in the 2-MDa cyanobacterial PSI-IsiA photosynthetic supercomplex observed using Cryo-EM, revealing large-scale variances in the positions of IsiA relative to PSI. Single-molecule measurements found efficient IsiA-to-PSI energy transfer across all conformations, along with signatures of transiently decoupled IsiA. Structure based calculations showed that rapid IsiA-to-PSI energy transfer is always maintained, and even increases by three-fold in rare conformations via IsiA-specific chls. We postulate that antennae design mitigates structural fluctuations, providing a mechanism for robust energy transfer in the flexible membrane.

Suggested Citation

  • Dvir Harris & Hila Toporik & Gabriela S. Schlau-Cohen & Yuval Mazor, 2023. "Energetic robustness to large scale structural fluctuations in a photosynthetic supercomplex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40146-8
    DOI: 10.1038/s41467-023-40146-8
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    References listed on IDEAS

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    1. Hila Toporik & Anton Khmelnitskiy & Zachary Dobson & Reece Riddle & Dewight Williams & Su Lin & Ryszard Jankowiak & Yuval Mazor, 2020. "Author Correction: The structure of a red-shifted photosystem I reveals a red site in the core antenna," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    2. Lars V. Bock & Helmut Grubmüller, 2022. "Effects of cryo-EM cooling on structural ensembles," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. E. J. Boekema & A. Hifney & A. E. Yakushevska & M. Piotrowski & W. Keegstra & S. Berry & K.-P. Michel & E. K. Pistorius & J. Kruip, 2001. "A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria," Nature, Nature, vol. 412(6848), pages 745-748, August.
    4. Hila Toporik & Anton Khmelnitskiy & Zachary Dobson & Reece Riddle & Dewight Williams & Su Lin & Ryszard Jankowiak & Yuval Mazor, 2020. "The structure of a red-shifted photosystem I reveals a red site in the core antenna," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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    Cited by:

    1. Xiuxiu Li & Guoqiang Huang & Lixia Zhu & Chenyang Hao & Sen-Fang Sui & Xiaochun Qin, 2024. "Structure of the red-shifted Fittonia albivenis photosystem I," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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