Orbital Configuration of the Valence Electrons, Ligand Field Symmetry, and Manganese Oxidation States of the Photosynthetic Water Oxidizing Complex: Analysis of the S2State Multiline EPR Signals

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Abstract
A theoretical framework is presented for analysis of all three “multiline” EPR spectra (MLS) arising from the tetramanganese (Mn4) cluster in the S2 oxidation state of the photosynthetic water oxidizing complex (WOC). Accurate simulations are presented which include anisotropy of the g and (four) 55Mn hyperfine tensors, chosen according to a database of 55Mn(III) and 55Mn(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” NH3-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 Mn4 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 Mn4 cluster proposed independently from Mn EXAFS studies. Simulated MLS were constructed for each of the eight (or seven) doublet states of the Mn4 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 |S12,S34,ST|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 NH3-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 Ca2+-depleted MLS suggests that Ca2+-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 NH3-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 d4 electron configuration of each Mn(III) ion corresponds to a flattened (oblate) ellipsoid. This electronic distribution is favored in five-coordinate ligand fields having trigonally compressed bipyramidal geometry, but it could also arise, in principle, in strained six-coordinate ligand fields having tetragonally compressed geometry, i.e. [Mn2(μ-O)]4+ (reverse Jahn−Teller distortion). The resulting valence electronic configurations are described as e‘2e‘‘2 and (dπ)3(dx2-y2)1, respectively, in contrast to the (dπ)3(dz2)1 configuration common to unstrained six-coordinate tetragonally-extended Mn(III) ions, such as found in the [Mn2(μ-O)2]3+ core in several synthetic dimers and catalase. Both of the former geometries predict strongly oxidizing Mn(III) ions, thereby suggesting a structural basis for the oxidative reactivity of the Mn4 cluster in the WOC. The magnetic model needed to explain the MLS is not readily reconciled with the simplest structural and electronic models deduced from EXAFS studies of the WOC.

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