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Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits

Nature Plants volume 5, pages 263–272 (2019)Cite this article

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Abstract

Photosystem I (PSI) is a highly efficient natural light-energy converter, and has diverse light-harvesting antennas associated with its core in different photosynthetic organisms. In green algae, an extremely large light-harvesting complex I (LHCI) captures and transfers energy to the PSI core. Here, we report the structure of PSI–LHCI from a green alga Bryopsis corticulans at 3.49 Å resolution, obtained by single-particle cryo-electron microscopy, which revealed 13 core subunits including subunits characteristic of both prokaryotes and eukaryotes, and 10 light-harvesting complex a (Lhca) antennas that form a double semi-ring and an additional Lhca dimer, including a novel four-transmembrane-helix Lhca. In total, 244 chlorophylls were identified, some of which were located at key positions for the fast energy transfer. These results provide a firm structural basis for unravelling the mechanisms of light-energy harvesting, transfer and quenching in the green algal PSI–LHCI, and important clues as to how PSI–LHCI has changed during evolution.

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Fig. 1: Overall structure of the PSI–LHCI supercomplex from B. corticulans.
Fig. 2: Structures of Lhcas.
Fig. 3: Interactions between the outer and inner Lhcas and between the additional Lhca dimers and the PSI core.
Fig. 4: Chlorophyll arrangement in the Lhca subunits of B. corticulans.
Fig. 5: Carotenoid arrangement in the green algal PSI–LHCI supercomplex.
Fig. 6: Possible energy-transfer pathways in the PSI–LHCI supercomplex of B. corticulans.
Fig. 7: Evolutionary scheme for the structural changes of PSI–LHCI from cyanobacteria to higher plants.

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Data availability

The cryo-EM density map and atomic models for the PSI–LHCI supercomplex structure at 3.49 Å have been deposited in the Electron Microscopy Data Bank and the Protein Data Bank under accession codes EMD-9670 and 6IGZ, respectively. The data that support the findings of this study are available from the corresponding authors upon reasonable request.

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Acknowledgements

We thank J. Lei and the staff at the Tsinghua University Branch of the National Center for Protein Sciences Beijing for providing facility support, and the Explorer 100 cluster system of the Tsinghua National Laboratory for Information Science and Technology for providing computation resources. We thank S. Qin and Z. Liu from Yantai Institute of Coastal Zone Research, CAS for assistance in collecting B. corticulans, L. Shu from Shanghai Luming Biotechnology for mass spectrometry analysis. The project was funded by the National Key R&D Program of China (2017YFA0503700, 2016YFA0501101, 2015CB150101); the National Natural Science Foundation of China (31622007, 31670237, 31600191); a Strategic Priority Research Program of CAS (XDB17000000); State Key Laboratory of Membrane Biology; and Taishan Scholars Project.

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Author notes

  1. These authors contributed equally: Xiaochun Qin, Xiong Pi.

Authors and Affiliations

  1. School of Biological Science and Technology, University of Jinan, Jinan, China

    Xiaochun Qin, Lixia Zhu & Mingmei Liu

  2. Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Xiaochun Qin, Wenda Wang, Guangye Han, Jian-Ren Shen & Tingyun Kuang

  3. State Key Laboratory of Membrane Biology, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing, China

    Xiong Pi, Linpeng Cheng & Sen-Fang Sui

  4. Institute for Interdisciplinary Science, Okayama University, Okayama, Japan

    Jian-Ren Shen

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Contributions

T.K. and S.-F.S. conceived the project; X.Q. performed the sample preparation, characterization and sequence analysis; X.P. processed the cryo-EM data, built and refined the structure model; W.W. and G.H. assisted in sample preparation; L.Z. and M.L. cloned Lhcas from B. corticulans and assisted in sequence analysis; X.Q. and X.P. analysed the structure; X.Q., X.P., J.-R.S., T.K. and S.-F.S. wrote the manuscript and all authors discussed and commented on the results and the manuscript.

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Correspondence to Tingyun Kuang or Sen-Fang Sui.

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Journal peer review information: Nature Plants thanks Egbert Boekema, Jean-David Rochaix and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Qin, X., Pi, X., Wang, W. et al. Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat. Plants 5, 263–272 (2019). https://doi.org/10.1038/s41477-019-0379-y

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