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Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Author

Listed:
  • Shiun-Jr Yang

    (University of California, Berkeley
    Lawrence Berkeley National Laboratory
    Kavli Energy Nanoscience Institute at Berkeley)

  • David J. Wales

    (University of Cambridge, Lensfield Road)

  • Esmae J. Woods

    (University of Cambridge, Lensfield Road
    University of Cambridge, JJ Thomson Avenue)

  • Graham R. Fleming

    (University of California, Berkeley
    Lawrence Berkeley National Laboratory
    Kavli Energy Nanoscience Institute at Berkeley)

Abstract

Photosystem II (PSII) has the unique ability to perform water-splitting. With light-harvesting complexes, it forms the PSII supercomplex (PSII-SC) which is a functional unit that can perform efficient energy conversion, as well as photoprotection, allowing photosynthetic organisms to adapt to the naturally fluctuating sunlight intensity. Achieving these functions requires a collaborative energy transfer network between all subunits of the PSII-SC. In this work, we perform kinetic analyses and characterise the energy landscape of the PSII-SC with a structure-based energy transfer model. With first passage time analyses and kinetic Monte Carlo simulations, we are able to map out the overall energy transfer network. We also investigate how energy transfer pathways are affected when individual protein complexes are removed from the network, revealing the functional roles of the subunits of the PSII-SC. In addition, we provide a quantitative description of the flat energy landscape of the PSII-SC. We show that it is a unique landscape that produces multiple kinetically relevant pathways, corresponding to a high pathway entropy. These design principles are crucial for balancing efficient energy conversion and photoprotection.

Suggested Citation

  • Shiun-Jr Yang & David J. Wales & Esmae J. Woods & Graham R. Fleming, 2024. "Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53138-z
    DOI: 10.1038/s41467-024-53138-z
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    References listed on IDEAS

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    1. Pavel Malý & Julian Lüttig & Peter A. Rose & Arthur Turkin & Christoph Lambert & Jacob J. Krich & Tobias Brixner, 2023. "Separating single- from multi-particle dynamics in nonlinear spectroscopy," Nature, Nature, vol. 616(7956), pages 280-287, April.
    2. Diego Prada-Gracia & Jesús Gómez-Gardeñes & Pablo Echenique & Fernando Falo, 2009. "Exploring the Free Energy Landscape: From Dynamics to Networks and Back," PLOS Computational Biology, Public Library of Science, vol. 5(6), pages 1-9, June.
    3. Davide Accomasso & Giacomo Londi & Lorenzo Cupellini & Benedetta Mennucci, 2024. "The nature of carotenoid S* state and its role in the nonphotochemical quenching of plants," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    4. David J. Wales & Mark A. Miller & Tiffany R. Walsh, 1998. "Archetypal energy landscapes," Nature, Nature, vol. 394(6695), pages 758-760, August.
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