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Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II

Nature volume 438, pages 1040–1044 (2005)Cite this article

Abstract

Oxygenic photosynthesis in plants, algae and cyanobacteria is initiated at photosystem II, a homodimeric multisubunit protein–cofactor complex embedded in the thylakoid membrane1. Photosystem II captures sunlight and powers the unique photo-induced oxidation of water to atmospheric oxygen1,2. Crystallographic investigations of cyanobacterial photosystem II have provided several medium-resolution structures (3.8 to 3.2 Å)3,4,5,6 that explain the general arrangement of the protein matrix and cofactors, but do not give a full picture of the complex. Here we describe the most complete cyanobacterial photosystem II structure obtained so far, showing locations of and interactions between 20 protein subunits and 77 cofactors per monomer. Assignment of 11 β-carotenes yields insights into electron and energy transfer and photo-protection mechanisms in the reaction centre and antenna subunits. The high number of 14 integrally bound lipids reflects the structural and functional importance of these molecules for flexibility within and assembly of photosystem II. A lipophilic pathway is proposed for the diffusion of secondary plastoquinone that transfers redox equivalents from photosystem II to the photosynthetic chain. The structure provides information about the Mn4Ca cluster, where oxidation of water takes place. Our study uncovers near-atomic details necessary to understand the processes that convert light to chemical energy.

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Figure 1: The PSII monomer from the cytoplasmic side.
Figure 2: The plastoquinone diffusion pathway.
Figure 3: Redox-active cofactors and electron transfer chain.
Figure 4: Oxygen-evolving centre.

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Acknowledgements

We thank D. DiFiore and C. Lüneberg for technical assistance; K.-D. Irrgang, H. Lokstein, J. Messinger, F. Müh, T. Renger, E. Schlodder and J. Yano for discussions; and R. Clarke, G. Renger, K. Sauer and V. Yachandra for critically reading the manuscript. Beam time and support at the ESRF, SLS, BESSY and DESY are gratefully acknowledged. We thank Deutsche Forschungsgemeinschaft and Fonds der Chemischen Industrie for support.

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Author notes

  1. Bernhard Loll

    Present address: Max-Planck-Institut für Medizinische Forschung, Abteilung für Biomolekulare Mechanismen, D-69120, Heidelberg, Germany

  2. Bernhard Loll 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, D-14195, Berlin, Germany

    Bernhard Loll, Wolfram Saenger & Jacek Biesiadka

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

    Jan Kern & Athina Zouni

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Corresponding authors

Correspondence to Wolfram Saenger or Athina Zouni.

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Competing interests

Atomic coordinates have been deposited in the Protein Data Bank under the accession number 2AXT. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1–7. (PDF 689 kb)

Supplementary Tables

This file contains Supplementary Tables 1–4. (PDF 38 kb)

Supplementary Methods

This file gives a detailed description about the structure determination and interpretation of the electron density maps, as well as calculation of electron transfer rates. (PDF 88 kb)

Supplementary Discussion

This file gives comparison to other published PSII structures and further details of the probable function of low molecular weight subunits, the protein environment of the non-haem Fe2+ and quinone binding pockets, as well as the carotenoids and the Mn4Ca-cluster. (PDF 102 kb)

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Loll, B., Kern, J., Saenger, W. et al. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044 (2005). https://doi.org/10.1038/nature04224

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