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A theoretical framework is presented for analysis of all three "multiline" EPR spectra (MLS) arising from the tetramanganese (Mn(4)) cluster in the S(2) oxidation state of the photosynthetic water oxidizing complex (WOC). Accurate simulations are presented which include anisotropy of the g and (four) (55)Mn hyperfine tensors, chosen according to a database of (55)Mn(III) and (55)Mn(IV) hyperfine tensors obtained previously using unbiased least-squares spectral fitting routines. In view of the large (30%) anisotropy common to Mn(III) hyperfine tensors in all complexes, previous MLS simulations which have assumed isotropic hyperfine constants have required physically unrealistic parameters. A simple model is found which offers good simulations of both the native "19-21-line" MLS and the "26-line" NH(3)-bound form of the MLS. Both a dimer-of-dimers and distorted-trigonal magnetic models are examined to describe the symmetry of the Heisenberg exchange interactions within the Mn(4) cluster and thus define the initial electronic basis states of the cluster. The effect of rhombic symmetry distortions is explicitly considered. Both magnetic models correspond to one of several possible structural models for the Mn(4) cluster proposed independently from Mn EXAFS studies. Simulated MLS were constructed for each of the eight (or seven) doublet states of the Mn(4) cluster in the WOC for the two viable oxidation models (3Mn(III)-1Mn(IV) or 3Mn(IV)-1Mn(III)), and using a wide range of axial Mn hyperfine tensors, with either coaxial or orthogonal tensor alignments. We find accurate simulations using the 3Mn(III)-1Mn(IV) oxidation model. In the dimer-of-dimers coupling model, the spin state conversion between two doublet states |S(12),S(34),S(T)|(7)/(2),4,(1)/(2)> and |(7)/(2),3,(1)/(2)> is found to explain the large (25%) contraction in the hyperfine splitting observed upon conversion from the native MLS to the NH(3)-bound MLS. Stabilization of this excited state as the new ground state is caused by change in the intermanganese exchange coupling, without appreciable change in the intrinsic hyperfine tensors. The lack of good simulations of the Ca(2+)-depleted MLS suggests that Ca(2+)-depletion changes both Mn ligation and intermanganese exchange coupling. The 3Mn(IV)-1Mn(III) oxidation model is disfavored because only approximate simulations could be found for the native MLS and no agreement with the NH(3)-bound MLS was obtained. The scalar part of the hyperfine tensors for both Mn(III) and Mn(IV) ions were found to approximate (+/-5%) the values for the dimanganese(III,IV) catalase enzyme, suggesting similar overall ligand types. However, the large (30%) anisotropic part of the Mn(III) hyperfine interaction is opposite in sign to that found in all tetragonally extended six-coordinate Mn(III) ions (i.e., the usual Jahn-Teller splitting). The distribution of spin density from the high-spin d(4) electron configuration of each Mn(III) ion corresponds to a flattened (oblate) ellipsoid. This electronic distribution is favored in five...

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Four of the five intermediate oxidation states (S-states) in the catalytic cycle of water oxidation used by O2-evolving photoautotrophs have been previously characterized by EPR and/or ENDOR spectroscopy, with the first reports for the S0, S1, and S3 states available in just the last three years. The first electron density map of the Mn cluster derived from X-ray diffraction measurements of single crystals of photosystem II at 3.8-4.2 A resolution has also appeared this year. This wealth of new information has provided significant insight into the structure of the inorganic core (Mn4OxCa1Cl1-2), the Mn oxidation states, and the location and function of the essential Ca2+ cofactor within the water-oxidizing complex (WOC). We summarize these advances and provide a unified interpretation of debated structural proposals and Mn oxidation states, based on an integrated analysis of the published data, particularly from Mn X-ray absorption spectroscopy (XAS) and EPR/ENDOR data. Only three magnetic spin-exchange models for the inter-manganese interactions are possible from consideration of the EPR data for the S0, S1, S2 and S(-N) (NO-reduced) states. These models fall into one of three types denoted butterfly, funnel, or tetrahedron. A revised set of eight allowed chemical structures for the Mn4Ox core can be deduced that are shown to be consistent with both EPR and XAS. The popular "dimer-of-dimers" structural model is not compatible with the possible structural candidates. EPR data have identified two inter-manganese couplings that are sensitive to the S-state, suggesting two possible bridging sites for substrate water molecules. Spin densities derived from 55Mn hyperfine data together with Mn K-edge energies from Ca-depleted samples provide an internally consistent assignment for the Mn oxidation states of Mn4(3III,IV) for the S2 state. EPR and XAS data also provide a consistent picture, locating Ca2+ as an integral part of the inorganic core, probably via shared bridging ligands with Mn (aqua/hydroxo/carboxylato/chloro). XAS data reveal that the Ca2+ cofactor increases the Mn(1s-->4p) transition energy by 0.6-1 eV with minimal structural perturbation versus the Ca-depleted WOC. Thus, calcium binding appears to increase the Mn-ligand covalency by increasing electron transfer from shared ligands to Mn, suggesting a direct role for Ca2+ in substrate water oxidation. Consideration of both the XAS and the EPR data, together with reactivity studies on two model complexes that evolve O2, suggest two favored structure types as feasible models for the reactive S4 state that is precursor to the O2 evolution step. These are a calcium-capped "cuboidal" core and a calcium-capped "funnel" core.

Photosynthesis produces molecular oxygen from water catalyzed by an enzyme whose active site contains a tetramanganese−oxo core of incompletely established structure. The first functional mimic of this core has been synthesized containing a cubical [Mn4O4] n + core, surrounded by six facially bridging bidentate chelates to the manganese ions ((dpp)6Mn4O4 (1); dpp- = diphenylphosphinate anion). Bond enthalpy data predict that the Mn4O4 6+ core is thermodynamically capable of releasing molecular O2, but is kinetically prevented from doing so by an activation barrier. UV light absorption into a Mn−O charge-transfer excited state (but not excitation of a Mn ligand-field excited state) efficiently releases an O2 molecule if performed in the gas phase and concomitantly releases a bridging dpp- anion and the cationic species (dpp)5Mn4O2 + (presumed Mn4O2-butterfly core type). All species were identified by high resolution mass spectrometry. This reaction proceeds with high quantum efficiency (>50%) and is the only observable reaction channel. The O2 product derived exclusively from the corner oxo's of the cube based on photochemistry of the 18O-isotopomer, ((dpp)6Mn4(18O)4. Neither O2 release nor dpp- dissociation are observed individually to occur in the excited state, indicating that O−O bond formation and O2 release require dissociation of one of the six dpp- chelates (“Jack-in-the-Box” mechanism for O2 formation). By contrast, neither O2 production nor chelate photodissociation are observed in condensed phases, presumably due to either quenching of the photoexcited state or rapid recombination of dpp- and (dpp)5Mn4O4 + in the solvent cage. Previous results show that chemical reduction of (1) in solution using hydrogen atom donors produces the deoxygenated (dpp)6Mn4O2 core and releases two water molecules as the only products. Thus the [Mn4O4] n + cubane core is an intrinsically reactive core topology that facilitates both the selective chemical reduction of two of the four oxygen atom bridges to water molecules and their photorearrangement to an O2 molecule under the control of chelation of the manganese ions by dpp-. These results may offer insight into the possible nature of the photosynthetic O2-evolving mechanism.