Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I

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Abstract

In plants and green algae, the core of photosystem I (PSI) is surrounded by a peripheral antenna system consisting of light-harvesting complex I (LHCI). Here we report the cryo-electron microscopic structure of the PSI–LHCI supercomplex from the green alga Chlamydomonas reinhardtii. The structure reveals that eight Lhca proteins form two tetrameric LHCI belts attached to the PsaF side while the other two Lhca proteins form an additional Lhca2/Lhca9 heterodimer attached to the opposite side. The spatial arrangement of light-harvesting pigments reveals that Chlorophylls b are more abundant in the outer LHCI belt than in the inner LHCI belt and are absent from the core, thereby providing the downhill energy transfer pathways to the PSI core. PSI–LHCI is complexed with a plastocyanin on the patch of lysine residues of PsaF at the luminal side. The assembly provides a structural basis for understanding the mechanism of light-harvesting, excitation energy transfer of the PSI–LHCI supercomplex and electron transfer with plastocyanin.

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Fig. 1: Cryo-EM structure of the PSI–LHCI supercomplex from C. reinhardtii.
Fig. 2: Cryo-EM density map and structure of the Lhca2/Lhca9 heterodimer.
Fig. 3: Comparison of the structures of five LHCI heterodimers.
Fig. 4: Comparison of the structures of green algal PSI–LHCI and red algal PSI–LHCR.
Fig. 5: Distribution of Chls a and b in green algal PSI–LHCI.
Fig. 6: Chlorophyll arrangement and plausible energy transfer pathways in the PSI–LHCI supercomplex.
Fig. 7: Extra density in the vicinity of the N-terminal helix of PsaF at the luminal side.

Data availability

Atomic coordinates of the green algal PSI–LHCI have been deposited in the Protein Data Bank with accession codes 6JO5 (PSI–10Lhca) and 6JO6 (PSI–8Lhca). Cryo-EM maps of green algal PSI–LHCI have been deposited in the Electron Microscopy Data Bank with accession codes EMD-9853 (map c2), EMD-9854 (map d), EMD-9855 (map a) and EMD-9856 (map b).

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Acknowledgements

We thank J.-R. Shen and K. Iwasaki for discussions, especially at the initial stage of the project. We also thank A. Watanabe, R. Tokutsu and J. Minagawa at the National Institute for Basic Biology for the valuable suggestion to use Amphipol in the PSI-LHCI preparations. This research was supported by the Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research) from AMED. This work was supported by JSPS KAKENHI (grant nos. JP16H06162 and JP16H06296 to M.S. and JP16H06554 to Y.T.). This work was also supported by JST, PREST (grant no. JP18069982 to M.S.).

Author information

M.S., N.M. and Y.T. conceived the project. S.-I.O. and K.Y.-M. prepared the samples. N.M. and F.A. collected the cryo-EM data. N.M. processed the cryo-EM data. M.S. built and refined the structure. M.S., S.-I.O. and Y.T. wrote the manuscript. All authors discussed and commented on the results and the manuscript.

Correspondence to Naoyuki Miyazaki or Yuichiro Takahashi.

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The authors declare no competing interests.

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Peer Review Information: Nature Plants thanks Alexey Amunts, Jean-David Rochaix and other anonymous reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–13, Supplementary Tables 1–7.

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Suga, M., Ozawa, S., Yoshida-Motomura, K. et al. Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I. Nat. Plants 5, 626–636 (2019) doi:10.1038/s41477-019-0438-4

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