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Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution

Nature volume 409, pages 739–743 (2001)Cite this article

Abstract

Oxygenic photosynthesis is the principal energy converter on earth. It is driven by photosystems I and II, two large protein–cofactor complexes located in the thylakoid membrane and acting in series. In photosystem II, water is oxidized; this event provides the overall process with the necessary electrons and protons, and the atmosphere with oxygen. To date, structural information on the architecture of the complex has been provided by electron microscopy of intact, active photosystem II at 15–30 Å resolution1, and by electron crystallography on two-dimensional crystals of D1-D2-CP47 photosystem II fragments without water oxidizing activity at 8 Å resolution2. Here we describe the X-ray structure of photosystem II on the basis of crystals fully active in water oxidation3. The structure shows how protein subunits and cofactors are spatially organized. The larger subunits are assigned and the locations and orientations of the cofactors are defined. We also provide new information on the position, size and shape of the manganese cluster, which catalyzes water oxidation.

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Figure 1: Electron densities of PSII after density modification and their interpretation.
Figure 2: Structure of PSII with assignment of protein subunits and cofactors.
Figure 3: Arrangement of cofactors of the electron transfer chain located in subunits D1 and D2.
Figure 4: Location and orientation of manganese cluster.

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References

  1. Nield, J. et al. Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allow for comparison of their oxygen-evolving complex organisation. J. Biol. Chem. 275, 27940–27946 (2000).

    CAS  PubMed  Google Scholar 

  2. Rhee, K.-H., Morris, E. P., Barber, J. & Kühlbrandt, W. Three-dimensional structure of photosystem II reaction centre at 8 Å resolution. Nature 396, 283–286 (1998).

    Article  ADS  CAS  Google Scholar 

  3. Zouni, A., Jordan, R., Schlodder, E., Fromme, P. & Witt, H. T. First photosystem II crystals capable of water oxidation. Biochim. Biophys. Acta 1457, 103–105 (2000).

    Article  CAS  Google Scholar 

  4. Witt, H. T. Primary reactions of oxygenic photosynthesis. Ber. BunsenGes. Phys. Chem. 100, 1923–1942 (1996).

    Article  CAS  Google Scholar 

  5. Zouni, A. et al. in Photosynthesis: Mechanisms and Effects (ed. Garab, G.) 925–928 (Kluwer Academic, Dordrecht, 1998).

    Book  Google Scholar 

  6. Barry, B. A., Boerner, R. J. & de Paula, J. C. in The Molecular Biology of Cyanobacteria (ed. Bryant, D. A.) 217–257 (Kluwer Academic, Dordrecht, 1994).

    Book  Google Scholar 

  7. Svensson, B. et al. A model for the photosystem II reaction center core including the structure of the primary donor P680. Biochemistry 35, 14486–14502 (1996).

    Article  CAS  Google Scholar 

  8. Xiong, J., Subramaniam, S. & Govindjee. A knowledge-based three dimensional model of the photosystem II reaction center of Chlamydomonas reinhardtii. Photosynth. Res. 56, 229–254 (1998).

    Article  CAS  Google Scholar 

  9. Michel, H. & Deisenhofer, J. Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry 27, 1–7 (1988).

    Article  CAS  Google Scholar 

  10. Schubert, W.-D. et al. A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J. Mol. Biol. 280, 297–314 (1998).

    CAS  Google Scholar 

  11. Harrer, R., Bassi, R., Testi, M. G. & Schäfer, C. Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. Eur. J. Biochem. 255, 196–205 (1998).

    Article  CAS  Google Scholar 

  12. Ishikawa, Y. et al. Turnover of the aggregates and cross-linked products of the D1 protein generated by acceptor-side photoinhibition of photosystem II. Biochim. Biophys. Acta 1413, 147–158 (1999).

    Article  CAS  Google Scholar 

  13. Rhee, K.-H. Three-dimensional Structure of Photosystem II Reaction Center by Electron Cryo-microscopy. Thesis, Univ. Heidelberg (1998).

  14. Tomo, T., Enami, I. & Satoh, K. Orientation and nearest neighbor analysis of psbI gene product in the photosystem II reaction center complex using bifunctional cross-linkers. FEBS Lett. 323, 15–18 (1993).

    Article  CAS  Google Scholar 

  15. Shi, L. X., Kim, S. J., Marchant, A., Robinson, C. & Schröder, W. P. Characterisation of the PsbX protein from photosystem II and light regulation of its gene expression in higher plants. Plant. Mol. Biol. 40, 737–744 (1999).

    Article  CAS  Google Scholar 

  16. Summer, E. J., Schmid, V. H., Bruns, B. U. & Schmidt, G. W. Requirement for the H phosphoprotein in photosystem II of Chlamydomonas reinhardtii. Plant. Physiol. 113, 1359–1368 (1997).

    Article  CAS  Google Scholar 

  17. Zheleva, D., Sharma, J., Panico, M., Morris, H. R. & Barber, J. Isolation and characterization of monomeric and dimeric CP47-reaction center photosystem II complexes. J. Biol. Chem. 273, 16122–16127 (1998).

    Article  CAS  Google Scholar 

  18. Mayers, S. R. et al. Further characterization of the psbH locus of Synechocystis sp. PCC 6803: inactivation of psbH impairs QA to QB electron transport in photosystem 2. Biochemistry 32, 1454–1465 (1993).

    Article  CAS  Google Scholar 

  19. Ahmed, A., Tajmir-Riahi, H. A. & Carpentier, R. A quantitative secondary structure analysis of the 33 kDa extrinsic polypeptide of photosystem II by FTIR spectroscopy. FEBS Lett. 363, 65–68 (1995).

    Article  CAS  Google Scholar 

  20. Ghanotakis, D. F., Tsiotis, G. & Bricker T. M. in Concepts in Photobiology: Photosynthesis and Photomorphogenesis (eds Singhal, G. S., Renger, G., Sopory, S. K., Irrgang, K.-D. & Govindjee) 264–291 (Narosa, New Delhi, 1999).

    Book  Google Scholar 

  21. Zech, S. G. et al. Pulsed EPR measurement of the distance between P680•- and QA•- in photosystem II. FEBS Lett. 414, 454–456 (1997).

    Article  CAS  Google Scholar 

  22. Schelvis, J. P. M., van Noort, P. I., Aartsma, T. J. & van Gorkom, H. J. Energy transfer, charge separation and pigment arrangement in the reaction center of Photosystem II. Biochim. Biophys. Acta 1184, 242–250 (1994).

    Article  CAS  Google Scholar 

  23. Ruffle, S., Hutchison, R. & Sayre, R. T. in Photosynthesis: Mechanisms and Effects (ed. Garab, G.) 1013–1016 (Kluwer Academic, Dordrecht, 1998).

    Book  Google Scholar 

  24. Buser, C. A., Diner, B. A. & Brudvig, G. W. Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. Biochemistry 31, 11449–11459 (1992).

    Article  CAS  Google Scholar 

  25. Yachandra, V. K., Sauer, K. & Klein, M. P. Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem. Rev. 96, 2927–2950 (1996).

    Article  CAS  Google Scholar 

  26. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1996).

    Article  Google Scholar 

  27. CCP4 Collaborative computational project number 4. The CCP4 suite: programmes for protein crystallography. Acta Cryst. D 50, 760–763 (1994).

    Article  Google Scholar 

  28. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47, 110–119 (1991).

    Article  Google Scholar 

  29. Esnouf, R. M. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graphics 15, 132–134 (1997).

    Article  CAS  Google Scholar 

  30. Merritt, E. A. & Bacon, D. J. Raster3D—photorealistic molecular graphics. Methods Enzymol. 277, 505–524 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Lüneberg, H. Schmidt and D. DiFiore for technical assistance, and W.-D. Schubert, R. Bittl, E. Schlodder, K. Irrgang and P. Jordan for discussions. Beamline assistance at DESY (Hamburg), ESRF (Grenoble) and Elettra (Trieste), and help of M. Burghammer with data collection at the manganese edge is gratefully acknowledged. We thank Egbert J. Boekema for providing us with electron micrographs of PSII. This work was supported by Deutsche Forschungsgemeinschaft, Sonderforschungsbereiche 312 and 498, BMBF (W.S.), and Fonds der Chemischen Industrie (W.S., H.-T.W., N.K. and P.F.).

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Authors and Affiliations

  1. Max-Volmer-Institut für Biophysikalische Chemie und Biochemie, Technische Universität Berlin, Strasse des 17, Juni 135, Berlin, D-10623, Germany

    Athina Zouni, Horst-Tobias Witt, Jan Kern & Petra Fromme

  2. Institut für Chemie, Kristallographie, Freie Universität Berlin, Takustrasse 6, Berlin, D-14195, Germany

    Norbert Krauss, Wolfram Saenger & Peter Orth

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  1. Athina Zouni
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Correspondence to Wolfram Saenger.

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Zouni, A., Witt, HT., Kern, J. et al. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739–743 (2001). https://doi.org/10.1038/35055589

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