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Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride

Nature Structural & Molecular Biology volume 16, pages 334–342 (2009)Cite this article

Abstract

Photosystem II (PSII) is a large homodimeric protein–cofactor complex located in the photosynthetic thylakoid membrane that acts as light-driven water:plastoquinone oxidoreductase. The crystal structure of PSII from Thermosynechococcus elongatus at 2.9-Å resolution allowed the unambiguous assignment of all 20 protein subunits and complete modeling of all 35 chlorophyll a molecules and 12 carotenoid molecules, 25 integral lipids and 1 chloride ion per monomer. The presence of a third plastoquinone QC and a second plastoquinone-transfer channel, which were not observed before, suggests mechanisms for plastoquinol-plastoquinone exchange, and we calculated other possible water or dioxygen and proton channels. Putative oxygen positions obtained from a Xenon derivative indicate a role for lipids in oxygen diffusion to the cytoplasmic side of PSII. The chloride position suggests a role in proton-transfer reactions because it is bound through a putative water molecule to the Mn4Ca cluster at a distance of 6.5 Å and is close to two possible proton channels.

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Figure 1: The homodimeric PSII complex.
Figure 2: Lipids in photosystem II.
Figure 3: The quinone exchange cavity in PSII.
Figure 4: The Mn4Ca cluster of PSII and the Cl− binding site.
Figure 5: Possible substrate and product channels to the lumen and Xe positions in PSII.

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Acknowledgements

The authors are grateful to the Deutsche Forschungsgemeinschaft for support within the framework of Sfb 498 (projects A4, C7). We also acknowledge W. Kabsch for help with XDS, W. Schröder for help with protein sequencing, P. Franke and C. Weise for MS data collection and J. Biesiadka for cooperation. We thank F. Müh, G. Renger, R. Clarke, V. Yachandra and K. Sauer for discussion and careful reading of the manuscript. Beam time and support at ESRF (Grenoble), SLS (Villigen) and BESSY (Berlin) is gratefully acknowledged.

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Author notes

  1. Jan Kern

    Present address: Present address: Physical Biosciences Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, Berkeley, 94720 California, USA.,

  2. Albert Guskov and Jan Kern: These authors contributed equally to this work.

Authors and Affiliations

  1. Institut für Chemie und Biochemie/Kristallographie, Freie Universität Berlin, Takustrasse 6, Berlin, D-14195, Germany

    Albert Guskov, Azat Gabdulkhakov & Wolfram Saenger

  2. Institut für Chemie/Max Volmer Laboratorium für Biophysikalische Chemie, Technische Universität Berlin, Strasse des 17. Juni 135, Berlin, D-10623, Germany

    Jan Kern, Matthias Broser & Athina Zouni

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Contributions

M.B., J.K. and A.Z. purified and crystallized the protein; A. Guskov, M.B., J.K. and A. Gabdulkhakov collected diffraction data; A. Guskov and A. Gabdulkhakov did structure determination and model building; A. Gabdulkhakov calculated channels; A. Guskov, J.K., M.B., A. Gabdulkhakov, A.Z. and W.S. designed experiments, analyzed data and prepared the manuscript.

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Correspondence to Athina Zouni or Wolfram Saenger.

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Guskov, A., Kern, J., Gabdulkhakov, A. et al. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16, 334–342 (2009). https://doi.org/10.1038/nsmb.1559

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