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

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 resolution, and by electron crystallography on two-dimensional crystals of D1-D2-CP47 photosystem II fragments without water oxidizing activity at 8 Å resolution. Here we describe the X-ray structure of photosystem II on the basis of crystals fully active in water oxidation. 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.

[1]  J. Barber,et al.  Isolation and Characterization of Monomeric and Dimeric CP47-Reaction Center Photosystem II Complexes* , 1998, The Journal of Biological Chemistry.

[2]  R L Stanfield,et al.  Roles for glycosylation of cell surface receptors involved in cellular immune recognition. , 1999, Journal of molecular biology.

[3]  J. Barber,et al.  Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allows for comparison of their oxygen-evolving complex organization. , 2000, The Journal of biological chemistry.

[4]  G. Singhal.  Concepts in photobiology : photosynthesis and photomorphogenesis , 1999 .

[5]  H. Witt.  Primary reactions of oxygenic photosynthesis , 1996 .

[6]  D. Kranz,et al.  Glycosylation of the T-cell antigen-specific receptor and its potential role in lectin-mediated cytotoxicity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Carpentier,et al.  A quantitative secondary structure analysis of the 33 kDa extrinsic polypeptide of photosystem II by FTIR spectroscopy , 1995, FEBS letters.

[8]  J. Trevillyan,et al.  Differential inhibition of T cell receptor signal transduction and early activation events by a selective inhibitor of protein-tyrosine kinase. , 1990, Journal of immunology.

[9]  Y. Yamamoto,et al.  Turnover of the aggregates and cross-linked products of the D1 protein generated by acceptor-side photoinhibition of photosystem II. , 1999, Biochimica et biophysica acta.

[10]  Collaborative Computational,et al.  The CCP4 suite: programs for protein crystallography. , 1994, Acta crystallographica. Section D, Biological crystallography.

[11]  T. Bringman,et al.  Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis. , 1990, Journal of neuroimmunology.

[12]  S. Leibler,et al.  Robustness in simple biochemical networks , 1997, Nature.

[13]  D. Bryant.  The Molecular Biology of Cyanobacteria , 1994, Advances in Photosynthesis.

[14]  K. A. Wall,et al.  Inhibitors of glycoprotein processing alter T-cell proliferative responses to antigen and to interleukin 2. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R M Esnouf,et al.  An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. , 1997, Journal of molecular graphics & modelling.

[16]  E A Merritt,et al.  Raster3D: photorealistic molecular graphics. , 1997, Methods in enzymology.

[17]  Mark M. Davis,et al.  Ligand-specific oligomerization of T-cell receptor molecules , 1997, Nature.

[18]  R. Cummings,et al.  A mouse lymphoma cell line resistant to the leukoagglutinating lectin from Phaseolus vulgaris is deficient in UDP-GlcNAc: alpha-D-mannoside beta 1,6 N-acetylglucosaminyltransferase. , 1982, The Journal of biological chemistry.

[19]  Susumu Tonegawa,et al.  High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice , 1994, Cell.

[20]  D. Cantrell,et al.  Networking Rho family GTPases in lymphocytes. , 1998, Immunity.

[21]  J. Zou,et al.  Improved methods for building protein models in electron density maps and the location of errors in these models. , 1991, Acta crystallographica. Section A, Foundations of crystallography.

[22]  Z. Otwinowski,et al.  Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[23]  T. Bricker,et al.  Polypeptides of Photosystem II: Structure and function , 1999 .

[24]  G. Garab,et al.  Photosynthesis: Mechanisms and Effects , 1998, Springer Netherlands.

[25]  P Tuffery,et al.  A model for the photosystem II reaction center core including the structure of the primary donor P680. , 1996, Biochemistry.

[26]  P. Fromme,et al.  First photosystem II crystals capable of water oxidation. , 2000, Biochimica et biophysica acta.

[27]  P. Fromme,et al.  A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. , 1998, Journal of molecular biology.

[28]  B. Diner,et al.  Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. , 1992, Biochemistry.

[29]  L. A. Lewis,et al.  Galectin-1 Induces Partial TCR ζ-Chain Phosphorylation and Antagonizes Processive TCR Signal Transduction1 , 2000, The Journal of Immunology.

[30]  S. Tonegawa,et al.  CD28 costimulation is crucial for the development of spontaneous autoimmune encephalomyelitis. , 1999, Journal of immunology.

[31]  J. D. Paula,et al.  The Use of Cyanobacteria in the Study of the Structure and Function of Photosystem II , 1994 .

[32]  James Barber,et al.  Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution , 1998, Nature.

[33]  J. Deisenhofer,et al.  Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II , 1988 .

[34]  É. Hideg,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. , 1993, Biochemistry.

[35]  T. Tomo,et al.  Orientation and nearest neighbor analysis of psbI gene product in the photosystem II reaction center complex using bifunctional cross‐linkers , 1993, FEBS letters.

[36]  T. Aartsma,et al.  Energy transfer, charge separation and pigment arrangement in the reaction center of Photosystem II , 1994 .

[37]  A. Smolyar,et al.  Atomic structure of an αβ T cell receptor (TCR) heterodimer in complex with an anti‐TCR Fab fragment derived from a mitogenic antibody , 1998, The EMBO journal.

[38]  P. Stewart,et al.  Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. , 1999, Journal of immunology.

[39]  R. Bassi,et al.  Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. , 1998, European journal of biochemistry.

[40]  W. Lubitz,et al.  Pulsed EPR measurement of the distance between P680 +· and QA −· in photosystem II , 1997, FEBS letters.

[41]  P. Warne,et al.  Stimulation of p21ras upon T-cell activation , 1990, Nature.

[42]  V. Yachandra,et al.  Manganese Cluster in Photosynthesis: Where Plants Oxidize Water to Dioxygen. , 1996, Chemical reviews.

[43]  J. Dennis,et al.  Suppression of tumor growth and metastasis in Mgat5-deficient mice , 2000, Nature Medicine.

[44]  G. Schmidt,et al.  Requirement for the H Phosphoprotein in Photosystem II of Chlamydomonas reinhardtii , 1997, Plant physiology.

[45]  P. Fromme,et al.  Characterization of single crystals of Photosystem II from the thermophilic cyanobacterium Synechococcus elongatus , 1998 .