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Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria

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Abstract

Two large protein-cofactor complexes, photosystem I and photosystem II, are the central components of photosynthesis in the thylakoid membranes. Here, we report the 2.37-Å structure of a tetrameric photosystem I complex from a heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Four photosystem I monomers, organized in a dimer of dimer, form two distinct interfaces that are largely mediated by specifically orientated polar lipids, such as sulfoquinovosyl diacylglycerol. The structure depicts a more closely connected network of chlorophylls across monomer interfaces than those seen in trimeric PSI from thermophilic cyanobacteria, possibly allowing a more efficient energy transfer between monomers. Our physiological data also revealed a functional link of photosystem I oligomerization to cyclic electron flow and thylakoid membrane organization.

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Fig. 1: Cryo-EM structure of the tetrameric PSI complex.
Fig. 2: Intermonomer interactions mediated by PSI subunits.
Fig. 3: Lipid–protein interactions in the tetramer.
Fig. 4: Time-course of the nonbonded interactions during the in silico assembly of PSI tetramer from monomers.
Fig. 5: Phenotype characterization of the WT and mutant strains of Anabaena 7120 under different light and nitrogen conditions.
Fig. 6: Thin-section EM images of the vegetative cells and heterocysts of Anabaena 7120.

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Data availability

Atomic coordinates have been deposited in the Protein Data Bank under the accession code 6K61. The cryo-EM density map has been uploaded to the Electron Microscopy Data Bank under the accession code EMD-9918. All other data can be obtained from the corresponding authors upon reasonable request.

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Acknowledgements

We thank the Electron Microscopy Laboratory of Peking University and the cryo-EM platform of Peking University for cryo-EM data collection. We also thank the Core Facilities at School of Life Sciences Peking University for assistance with thin-section EM sample preparation and image analysis. The computation was supported by High-Performance Computing Platform of Peking University. The work was funded by the Ministry of Science and Technology of China (grant nos. 2016YFA0500700 to N.G. and 2015CB150101 and 2017YFA503703 to J.Z.), the National Natural Science Foundation of China (grant nos. 31725007 and 31630087 to N.G., 91851118 to J.Z., and 21625302 and 21573217 to G.L.).

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  1. These authors contributed equally: Lvqin Zheng, Yanbing Li, Xiying Li.

Authors and Affiliations

  1. State Key Laboratory of Membrane Biology, Peking–Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, School of Life Sciences, Peking University, Beijing, China

    Lvqin Zheng, Ningning Li, Chengying Ma & Ning Gao

  2. State Key Laboratory of Protein and Plant Genetic Engineering, School of Life Sciences, Peking University, Beijing, China

    Yanbing Li, Xiying Li, Kun Zhang & Jindong Zhao

  3. State Key Laboratory of Molecular Reaction Dynamics, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian, China

    Qinglu Zhong, Yuebin Zhang, Huiying Chu & Guohui Li

  4. Chinese Academy of Sciences Key Laboratory of Phycological Research, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, China

    Jindong Zhao

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Contributions

N.G. and J.Z. conceived the project. Y.L. purified photosystem I samples. L.Z. and Y.L. collected cryo-EM data. L.Z., C.M. and N.L. processed the cryo-EM data. L.Z., Y.L., X.L. and K.Z. conducted biochemical analysis. G.L. designed the MD strategy. G.L., Q.Z., Y.Z. and H.C. performed simulations. G.L. and Q.Z. analysed the simulation data. L.Z., Y.L., G.L., N.G. and J.Z. wrote the manuscript. All authors discussed and commented on the results and the manuscript.

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Correspondence to Guohui Li, Jindong Zhao or Ning Gao.

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Zheng, L., Li, Y., Li, X. et al. Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria. Nat. Plants 5, 1087–1097 (2019). https://doi.org/10.1038/s41477-019-0525-6

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