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X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex

Nature Plants volume 4, pages 218–224 (2018)Cite this article

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Abstract

Photosystem I (PSI), a large protein complex located in the thylakoid membrane, mediates the final step in light-driven electron transfer to the stromal electron carrier protein ferredoxin (Fd). Here, we report the first structural description of the PSI–Fd complex from Thermosynechococcus elongatus. The trimeric PSI complex binds three Fds in a non-equivalent manner. While each is recognized by a PSI protomer in a similar orientation, the distances between Fds and the PSI redox centres differ. Fd binding thus entails loss of the exact three-fold symmetry of the PSI’s soluble subunits, inducing structural perturbations which are transferred to the lumen through PsaF. Affinity chromatography and nuclear magnetic resonance analyses of PSI–Fd complexes support the existence of two different Fd-binding states, with one Fd being more tightly bound than the others. We propose a dynamic structural basis for productive complex formation, which supports fast electron transfer between PSI and Fd.

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Fig. 1: Overall structure of the cyanobacterial PSI–Fd complex.
Fig. 2: Intermolecular interactions between Fd and PSI.
Fig. 3: NMR chemical shift perturbation.
Fig. 4: Structural changes in PSI induced by Fd binding calculated from the Fd-free PSI structure (PDB ID: 1JB0).
Fig. 5: Structural differences between the Fd-bound PSI trimer and the corresponding PSI monomer.

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Acknowledgements

We thank T. Hase for valuable discussions on the Fd-affinity chromatography; T. Kikuchi, P. Liauw, Y. Takagi, E. El-Mohsnawy, N. Muraki and T. Oyama for technical help in the initial stage of this project; E. Yamashita, A. Higashiura and A. Nakagawa at SPring-8, Harima, Japan; and the staff at the Taiwan Light Source, Hsinchu, Taiwan, R.O.C for support during data collection. This work was supported by the Funding Programme for Next Generation World-Leading Researchers (GS016) from the Cabinet Office of Japan (G.K.) and an International Joint Research Promotion Programme, Osaka University (G.K. and M.R.).

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Author notes

  1. Hisako Kubota-Kawai

    Present address: National Institute for Basic Biology, Aichi, Japan

  2. Risa Mutoh

    Present address: Department of Applied Physics, Faculty of Science, Fukuoka University, Fukuoka, Japan

Authors and Affiliations

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

    Hisako Kubota-Kawai, Risa Mutoh, Kanako Shinmura, Hideaki Tanaka & Genji Kurisu

  2. Institut de Biologie Intégrative de la Cellule (I2BC), IBITECS, CEA, CNRS, Université Paris-Saclay, Gif-sur-Yvette, France

    Pierre Sétif

  3. Plant Biochemistry, Faculty of Biology & Biotechnology, Ruhr University Bochum, Bochum, Germany

    Marc M. Nowaczyk & Matthias Rögner

  4. Graduate School of Medical Life Science, Yokohama City University, Yokohama, Japan

    Takahisa Ikegami

  5. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan

    Takahisa Ikegami, Hideaki Tanaka & Genji Kurisu

  6. Department of Macromolecular Science, Graduate School of Science, Osaka, Japan

    Hideaki Tanaka & Genji Kurisu

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Contributions

Purification of WTFd was conducted by K.S. Preparation of GaFd was conducted by R.M. Purification of His-tagged PSI was introduced for structural analysis by H.K.-K., M.N. and M.R. Flash-absorption spectroscopy was carried out by P.S. Crystallization and X-ray data collection of PSI–Fd complexes were conducted by H.K-K. The crystal structures of PSI–Fd were solved by H.T., H.K-K. and G.K. NMR analysis was done by R.M. and T.I. G.K. contributed to the design of the experiments and writing the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Genji Kurisu.

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Supplementary Information

Supplementary Figures 1–7 and Supplementary Table 1.

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Supplementary GIF 1

Top view of the superimposed models of the free PSI coloured in grey and the Fd-bound PSI trimer in dark green. Each Fd molecule is coloured in yellow, green and cyan.

Supplementary GIF 2

Side view of the same superimposed models of Supplementary GIF 1.

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Kubota-Kawai, H., Mutoh, R., Shinmura, K. et al. X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex. Nature Plants 4, 218–224 (2018). https://doi.org/10.1038/s41477-018-0130-0

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