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Structural basis for energy harvesting and dissipation in a diatom PSII–FCPII supercomplex

Nature Plants volume 5, pages 890–901 (2019)Cite this article

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Abstract

Light-harvesting antenna systems in photosynthetic organisms harvest solar energy and transfer it to the photosynthetic reaction centres to initiate charge-separation and electron-transfer reactions. Diatoms are one of the important groups of oxyphototrophs and possess fucoxanthin chlorophyll a/c-binding proteins (FCPs) as light harvesters. The organization and association pattern of FCP with the photosystem II (PSII) core are unknown. Here we solved the structure of PSII–FCPII supercomplexes isolated from a diatom, Chaetoceros gracilis, by single-particle cryoelectron microscopy. The PSII–FCPII forms a homodimer. In each monomer, two FCP homotetramers and three FCP monomers are associated with one PSII core. The structure reveals a highly complicated protein–pigment network that is different from the green-type light-harvesting apparatus. Comparing these two systems allows the identification of energy transfer and quenching pathways. These findings provide structural insights into not only excitation-energy transfer mechanisms in the diatom PSII–FCPII, but also changes of light harvesters between the red- and green-lineage oxyphototrophs during evolution.

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Fig. 1: Overall structure of the PSII–FCPII supercomplex.
Fig. 2: Structure of the FCP S-tetramer.
Fig. 3: Structural comparisons among different FCP monomers.
Fig. 4: Pigment–pigment interactions among different FCP units.
Fig. 5: Interactions between FCPII and the PSII cores.
Fig. 6: Possible excitation-energy transfer pathways in PSII–FCPII.
Fig. 7: Structural comparisons between the FCPII tetramer and LHCII trimer (the S-trimer in the PSII–LHCII complex (PDB 5XNL)).

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Data availability

Atomic coordinates and Cyro-EM maps for the reported structure of C2S2, C2S1M1 and C2S2M2 have been deposited in the Protein Data Bank under accession codes 6J3Y, 6J3Z and 6J40, respectively, and in the Electron Microscopy Data Bank under accession codes EMD-9775, EMD-9776 and EMD-9777, respectively.

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Acknowledgements

This work was supported by the Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from AMED under Grant No. JP18am0101072j0001 (to N.M.), PRESTO from JST Grant No. JPMJPR16P1 (to F.A.), JSPS KAKENHI Nos. JP17K07442 (to R.N.), JP16H06553 (to S.A.) and JP17H06433 (to J.-R.S.), Advanced Low Carbon Technology Research and Development Program from the Japan Science and Technology Agency Grant No. JPMJAL1105 (to Y.K. and K.I.) and a Collaborative Research Program from National Institute for Basic Biology Grant No. 18-451 (to K.I.). We thank H. Nishide, NIBB, for supporting the genome data analysis.

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Author notes

  1. These authors contributed equally: Ryo Nagao, Koji Kato.

Authors and Affiliations

  1. Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University, Okayama, Japan

    Ryo Nagao, Koji Kato, Jian-Ren Shen & Fusamichi Akita

  2. Biomolecular Characterization Unit, RIKEN Center for Sustainable Resource Science, Saitama, Japan

    Takehiro Suzuki & Naoshi Dohmae

  3. Graduate School of Biostudies, Kyoto University, Kyoto, Japan

    Kentaro Ifuku

  4. National Institute for Basic Biology, National Institutes of Natural Sciences, Aichi, Japan

    Ikuo Uchiyama

  5. Graduate School of Life Science, University of Hyogo, Hyogo, Japan

    Yasuhiro Kashino

  6. Graduate School of Science, Kobe University, Hyogo, Japan

    Seiji Akimoto

  7. Institute for Protein Research, Osaka University, Osaka, Japan

    Naoyuki Miyazaki

  8. Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance, University of Tsukuba, Ibaraki, Japan

    Naoyuki Miyazaki

  9. Japan Science and Technology Agency, PRESTO, Saitama, Japan

    Fusamichi Akita

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Contributions

R.N., J.-R.S., N.M. and F.A. conceived the project. R.N. purified the PSII–FCPII supercomplexes and performed their biochemical and spectroscopic characterizations. T.S. and N.D. identified gene products of FCP by MS analyses. K.I, I.U. and Y.K. provided genome information of C. gracilis. N.M. collected cryo-EM images. R.N., F.A. and N.M. processed the EM data. N.M. reconstructed the final EM maps. R.N., F.A., K.K. and N.M. built the structure model. K.K. refined the final models. F.A. analysed the structure. R.N. and S.A. proposed structural interpretation on the basis of spectroscopic analyses. R.N., F.A., K.K., S.A., N.M. and J.-R.S. wrote the paper. All of the authors contributed to the interpretations of the results and improvement of the manuscript.

Corresponding authors

Correspondence to Jian-Ren Shen, Naoyuki Miyazaki or Fusamichi Akita.

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Peer review information: Nature Plants thanks Douglas Campbell and Paul Jensen and other, anonymous, reviewers for their contribution to the peer review of this work

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Nagao, R., Kato, K., Suzuki, T. et al. Structural basis for energy harvesting and dissipation in a diatom PSII–FCPII supercomplex. Nat. Plants 5, 890–901 (2019). https://doi.org/10.1038/s41477-019-0477-x

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