Density functional calculations of (55)Mn, (14)N and (13)C electron paramagnetic resonance parameters support an energetically feasible model system for the S(2) state of the oxygen-evolving complex of photosystem II.

Metal and ligand hyperfine couplings of a previously suggested, energetically feasible Mn(4)Ca model cluster (SG2009(-1)) for the S(2) state of the oxygen-evolving complex (OEC) of photosystem II (PSII) have been studied by broken-symmetry density functional methods and compared with other suggested structural and spectroscopic models. This was carried out explicitly for different spin-coupling patterns of the S=1/2 ground state of the Mn(III)(Mn(IV))(3) cluster. By applying spin-projection techniques and a scaling of the manganese hyperfine couplings, computation of the hyperfine and nuclear quadrupole coupling parameters allows a direct evaluation of the proposed models in comparison with data obtained from the simulation of EPR, ENDOR, and ESEEM spectra. The computation of (55)Mn hyperfine couplings (HFCs) for SG2009(-1) gives excellent agreement with experiment. However, at the current level of spin projection, the (55)Mn HFCs do not appear sufficiently accurate to distinguish between different structural models. Yet, of all the models studied, SG2009(-1) is the only one with the Mn(III) site at the Mn(C) center, which is coordinated by histidine (D1-His332). The computed histidine (14)N HFC anisotropy for SG2009(-1) gives much better agreement with ESEEM data than the other models, in which Mn(C) is an Mn(IV) site, thus supporting the validity of the model. The (13)C HFCs of various carboxylates have been compared with (13)C ENDOR data for PSII preparations with (13)C-labelled alanine.

[1]  D. Gatteschi,et al.  EPR of Exchange Coupled Systems , 2012 .

[2]  Per E M Siegbahn,et al.  An energetic comparison of different models for the oxygen evolving complex of photosystem II. , 2009, Journal of the American Chemical Society.

[3]  P. Siegbahn.  Structures and energetics for O2 formation in photosystem II. , 2009, Accounts of chemical research.

[4]  M. Kaupp,et al.  Validation of broken-symmetry density functional methods for the calculation of electron paramagnetic resonance parameters of dinuclear mixed-valence MnIVMnIII complexes , 2009 .

[5]  M. Orio,et al.  Magnetic and spectroscopic properties of mixed valence manganese(III,IV) dimers: a systematic study using broken symmetry density functional theory. , 2009, Inorganic chemistry.

[6]  M. Orio,et al.  Structure of the oxygen-evolving complex of photosystem II: information on the S(2) state through quantum chemical calculation of its magnetic properties. , 2009, Physical chemistry chemical physics : PCCP.

[7]  A. Zouni,et al.  Electronic structure of the tyrosine D radical and the water-splitting complex from pulsed ENDOR spectroscopy on photosystem II single crystals. , 2009, Physical chemistry chemical physics : PCCP.

[8]  M. Orio,et al.  A new quantum chemical approach to the magnetic properties of oligonuclear transition-metal complexes: application to a model for the tetranuclear manganese cluster of photosystem II. , 2009, Chemistry.

[9]  C. Cummins,et al.  Two-electron reduction of a vanadium(V) nitride by CO to release cyanate and open a coordination site. , 2009, Journal of the American Chemical Society.

[10]  P. Siegbahn.  A structure-consistent mechanism for dioxygen formation in photosystem II. , 2008, Chemistry.

[11]  R. Debus,et al.  Multifrequency electron spin-echo envelope modulation studies of nitrogen ligation to the manganese cluster of photosystem II , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  P. Siegbahn.  Mechanism and energy diagram for O–O bond formation in the oxygen-evolving complex in photosystem II , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  M. Haumann,et al.  On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic-resolution models for four S-states , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  F. Neese,et al.  Focusing the view on nature's water-splitting catalyst , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  P. Siegbahn.  Theoretical studies of O-O bond formation in photosystem II. , 2008, Inorganic chemistry.

[16]  J. Yano,et al.  Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy. , 2008, Inorganic chemistry.

[17]  J. Barber.  Crystal structure of the oxygen-evolving complex of photosystem II. , 2008, Inorganic chemistry.

[18]  R. D. Britt,et al.  Multifrequency pulsed electron paramagnetic resonance study of the S2 state of the photosystem II manganese cluster. , 2008, Inorganic chemistry.

[19]  M. Kaupp,et al.  Structure and electron paramagnetic resonance parameters of the manganese site of concanavalin A studied by density functional methods , 2008 .

[20]  Holger Dau,et al.  The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level , 2008 .

[21]  T. Noguchi.  Fourier transform infrared analysis of the photosynthetic oxygen-evolving center , 2008 .

[22]  J. Barber,et al.  Revealing the structure of the Mn-cluster of photosystem II by X-ray crystallography , 2008 .

[23]  F. Neese,et al.  A systematic density functional study of the zero-field splitting in Mn(II) coordination compounds. , 2008, Inorganic chemistry.

[24]  W. Lubitz,et al.  Electronic structure of the Mn4OxCa cluster in the S0 and S2 states of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR spectroscopy. , 2007, Journal of the American Chemical Society.

[25]  Martin Kaupp,et al.  Density functional study of EPR parameters and spin-density distribution of azurin and other blue copper proteins. , 2007, The journal of physical chemistry. B.

[26]  A. Haddy.  EPR spectroscopy of the manganese cluster of photosystem II , 2007, Photosynthesis Research.

[27]  T. Noguchi,et al.  Drastic changes in the ligand structure of the oxygen-evolving Mn cluster upon Ca2+ depletion as revealed by FTIR difference spectroscopy. , 2007, Biochimica et biophysica acta.

[28]  M. Haumann,et al.  Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution , 2007, Photosynthesis Research.

[29]  Mitsutaka Okumura,et al.  A general algorithm for calculation of Heisenberg exchange integrals J in multispin systems , 2006 .

[30]  W. Saenger,et al.  Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn4Ca Cluster , 2006, Science.

[31]  N. Lewis,et al.  Powering the planet: Chemical challenges in solar energy utilization , 2006, Proceedings of the National Academy of Sciences.

[32]  Holger Dau,et al.  Rapid Loss of Structural Motifs in the Manganese Complex of Oxygenic Photosynthesis by X-ray Irradiation at 10–300 K* , 2006, Journal of Biological Chemistry.

[33]  Jan Kern,et al.  Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II , 2005, Nature.

[34]  K. Wieghardt,et al.  High‐field EPR investigations of MnIIIMnIV and MnIIMnIII states of dimanganese catalase and related model systems , 2005, Magnetic resonance in chemistry : MRC.

[35]  M. Grabolle,et al.  Photosynthetic O2 Formation Tracked by Time-Resolved X-ray Experiments , 2005, Science.

[36]  Uwe Bergmann,et al.  X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A. Boussac,et al.  Towards a spin coupling model for the Mn4 cluster in Photosystem II. , 2005, Biochimica et biophysica acta.

[38]  F. Neese,et al.  Dimanganese catalase—spectroscopic parameters from broken-symmetry density functional theory of the superoxidized MnIII/MnIV state , 2005, JBIC Journal of Biological Inorganic Chemistry.

[39]  W. Lubitz,et al.  55Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in photosystem II. , 2005, Journal of the American Chemical Society.

[40]  M. Haumann,et al.  The structure of the manganese complex of Photosystem II in its dark-stable S1-state?EXAFS results in relation to recent crystallographic data , 2004 .

[41]  M. Bühl,et al.  Calculation of NMR and EPR parameters : theory and applications , 2004 .

[42]  M. Kaupp,et al.  Spin-orbit effects on hyperfine coupling tensors in transition metal complexes using hybrid density functionals and accurate spin-orbit operators , 2004 .

[43]  R. D. Britt,et al.  Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. , 2004, Biochimica et biophysica acta.

[44]  James Barber,et al.  Architecture of the Photosynthetic Oxygen-Evolving Center , 2004, Science.

[45]  F. Neese,et al.  Calculating the electron paramagnetic resonance parameters of exchange coupled transition metal complexes using broken symmetry density functional theory: application to a MnIII/MnIV model compound. , 2004, Journal of the American Chemical Society.

[46]  M. Kaupp,et al.  Relativistic spin-orbit effects on hyperfine coupling tensors by density-functional theory. , 2004, The Journal of chemical physics.

[47]  G. Scuseria,et al.  Comparative assessment of a new nonempirical density functional: Molecules and hydrogen-bonded complexes , 2003 .

[48]  F. Neese.  Metal and ligand hyperfine couplings in transition metal complexes: The effect of spin-orbit coupling as studied by coupled perturbed Kohn-Sham theory , 2003 .

[49]  W. Lubitz,et al.  Multifrequency EPR Investigation of Dimanganese Catalase and Related Mn(III)Mn(IV) Complexes , 2003 .

[50]  Nobuo Kamiya,et al.  Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. Mulkidjanian,et al.  Electrostatics and proton transfer in photosynthetic water oxidation. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  Petra Fromme,et al.  Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution , 2001, Nature.

[53]  R. D. Britt,et al.  EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. , 2001, Biochimica et biophysica acta.

[54]  M. Kaupp,et al.  Mechanisms of EPR Hyperfine Coupling in Transition Metal Complexes , 2000 .

[55]  R. D. Britt,et al.  55Mn ENDOR of the S2-State Multiline EPR Signal of Photosystem II: Implications on the Structure of the Tetranuclear Mn Cluster , 2000 .

[56]  Martin Kaupp,et al.  A Critical Validation of Density Functional and Coupled-Cluster Approaches for the Calculation of EPR Hyperfine Coupling Constants in Transition Metal Complexes , 1999 .

[57]  E Schlodder,et al.  Stoichiometry of Proton Release from the Catalytic Center in Photosynthetic Water Oxidation , 1999, The Journal of Biological Chemistry.

[58]  M. Chan,et al.  Pulsed 1H and 55Mn ENDOR studies of dinuclear Mn(III)Mn(IV) model complexes , 1998 .

[59]  Christel M. Marian,et al.  A mean-field spin-orbit method applicable to correlated wavefunctions , 1996 .

[60]  M. Chan,et al.  55Mn ESE-ENDOR of a Mixed Valence Mn(III)Mn(IV) Complex: Comparison with the Mn Cluster of the Photosynthetic Oxygen-Evolving Complex , 1995 .

[61]  D. Case,et al.  Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters , 1995 .

[62]  M. Frisch,et al.  Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields , 1994 .

[63]  R. D. Britt,et al.  Temperature-dependent pulsed electron paramagnetic resonance studies of the S2 state multiline signal of the photosynthetic oxygen-evolving complex. , 1994, Biochemistry.

[64]  A. Becke.  Density-functional thermochemistry. III. The role of exact exchange , 1993 .

[65]  Hans W. Horn,et al.  Fully optimized contracted Gaussian basis sets for atoms Li to Kr , 1992 .

[66]  R. Pace,et al.  EPR saturation and temperature dependence studies on signals from the oxygen-evolving centre of photosystem II , 1991 .

[67]  G. Blondin,et al.  Interplay of Electron Exchange and Electron Transfer in Metal Polynuclear Complexes in Proteins or Chemical Models , 1990 .

[68]  Hans W. Horn,et al.  ELECTRONIC STRUCTURE CALCULATIONS ON WORKSTATION COMPUTERS: THE PROGRAM SYSTEM TURBOMOLE , 1989 .

[69]  A. Rutherford,et al.  EPR studies of the oxygen-evolving enzyme of Photosystem II , 1984 .

[70]  J. Casey,et al.  EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution , 1984 .

[71]  Louis Noodleman,et al.  Valence bond description of antiferromagnetic coupling in transition metal dimers , 1981 .

[72]  G. Dismukes,et al.  EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts , 1980 .

[73]  C. Ashby,et al.  CRYSTAL STRUCTURE AND NITROGEN-14 NUCLEAR QUADRUPOLE RESONANCE SPECTRUM OF CATENA-μ-IMIDAZOLATOBIS(IMIDAZOLE)ZINC NITRATE. DONOR CHARACTERISTICS OF COORDINATED IMIDAZOLATE , 1978 .

[74]  C. Ashby,et al.  Crystal structure and nitrogen-14 nuclear quadrupole resonance spectrum of catena-.mu.-imidazolatobis(imidazole)zinc nitrate. Donor characteristics of coordinated imidazolate , 1978 .

[75]  B. Forbush,et al.  COOPERATION OF CHARGES IN PHOTOSYNTHETIC O2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM , 1970, Photochemistry and photobiology.

[76]  J. Lavergne,et al.  Proton release during the redox cycle of the water oxidase , 2004, Photosynthesis Research.

[77]  G. Dismukes,et al.  Electronic structure of dimanganese(II,III) and dimanganese(III,IV) complexes and dimanganese catalase enzyme: a general EPR spectral simulation approach , 1994 .

[78]  N. Atherton,et al.  Principles of electron spin resonance , 1993 .

[79]  D. Collison,et al.  Electron paramagnetic resonance of d transition metal compounds , 1992 .

[80]  B. Guigliarelli,et al.  THE MIXED-VALENCE FE(III), FE(II) BINUCLEAR CENTERS OF BIOLOGICAL MOLECULES VIEWED THROUGH EPR SPECTROSCOPY , 1991 .

[81]  G. Dismukes,et al.  Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[82]  E. M. Loebl,et al.  Theoretical foundations of electron spin resonance , 1978 .

[83]  Peter Diehl,et al.  NMR: Basic Principles and Progress , 1969 .