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Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex

Abstract

During oxygenic photosynthesis, photosystems I and II (PSI and PSII) are essential for light-driven electron transport. Excitation energy transfer in PSI occurs extremely quickly, making it an efficient energy converter. In the alga Chlamydomonas reinhardtii (Cr), multiple units of light-harvesting complex I (LHCI) bind to the PSI core and function as peripheral antennae, forming a PSI–LHCI supercomplex. CrPSI–LHCI shows significantly larger antennae compared with plant PSI–LHCI while maintaining highly efficient energy transfer from LHCI to PSI. Here, we report structures of CrPSI–LHCI, solved by cryo-electron microscopy, revealing that up to ten LHCIs are associated with the PSI core. The structures provide detailed information about antenna organization and pigment arrangement within the supercomplexes. Highly populated and closely associated chlorophylls in the antennae explain the high efficiency of light harvesting and excitation energy transfer in CrPSI–LHCI.

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Fig. 1: The C. reinhardtii PSI–8LHCI supercomplex.
Fig. 2: The C. reinhardtii PSI–10LHCI supercomplex.
Fig. 3: Structure of the Lhca proteins in the PSI–8LHCI supercomplex.
Fig. 4: Comparison of Lhca proteins in the PSI–8LHCI supercomplex.
Fig. 5: Plausible energy transfer pathways within LHCI belts or from LHCI to the core in the PSI–8LHCI supercomplex.

Data availability

The atomic coordinates of the PSI–LHCI supercomplexes have been deposited in the PDB under accession codes 6IJJ (for PSI–8LHCI) and 6IJO (for PSI–10LHCI). The cryo-EM maps of these supercomplexes have been deposited in the EMDB with accession codes EMD-9678 (for PSI–8LHCI) and EMD-9680 (for PSI–10LHCI), respectively. All other data generated or analysed are available from the corresponding authors on reasonable request.

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Acknowledgements

Cryo-EM data collection was carried out at the Center for Biological Imaging, Core Facilities for Protein Science at the Institute of Biophysics, Chinese Academy of Sciences. We thank W. Yang from the Institute of Botany, Chinese Academy of Sciences, for providing the C. reinhardtii CC-124 strain; B. Zhu, X. Huang, G. Ji, D. Fan, T. Niu, F. Sun and other staff members at the Center for Biological Imaging for their support in data collection; L. Niu, X. Ding, M. Zhang and F. Yang for mass spectrometry; and L. Kong for cryo-EM data storage and backup. The project was funded by the National Key R&D Program of China (nos. 2017YFA0504700, 2017YFA0503702 and 2016YFA0502900), the Strategic Priority Research Program at the Chinese Academy of Sciences (nos. XDB08020302, XDB08030204 and XDB27020106), the Key Research Program of Frontier Sciences at the Chinese Academy of Sciences (no. QYZDB-SSW-SMC005) and the National Natural Science Foundation of China (nos. 31770778, 31700649 and 31600609). Z.L. and X. Zhang received scholarships from the ‘National Thousand Young Talents Program’ from the Office of Global Experts Recruitment in China. X.S., X.P. and J.M. were sponsored by the Youth Innovation Promotion Association at the Chinese Academy of Sciences.

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Contributions

M.L., W.C. and X.Zhang conceived the project. X.Zhao cultured the algae. X.S. performed sample preparation and characterization. X.S. and X.P. collected the cryo-EM data. J.M. and X.Zhang processed the cryo-EM data and reconstructed the cryo-EM maps. X.P. built and refined the structure model. X.P., M.L., X.Zhang and Z.L. analysed the structure. M.L., X.Zhang and Z.L. wrote the manuscript. All authors discussed and commented on the results and the manuscript.

Corresponding authors

Correspondence to Xinzheng Zhang or Mei Li.

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

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Su, X., Ma, J., Pan, X. et al. Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex. Nat. Plants 5, 273–281 (2019). https://doi.org/10.1038/s41477-019-0380-5

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