ELECTRONIC-STRUCTURE OF DIMANGANESE(II,III) AND DIMANGANESE(III,IV) COMPLEXES AND DIMANGANESE CATALASE ENZYME - A GENERAL EPR SPECTRAL SIMULATION APPROACH

A general approach for simulation of EPR spectra of mixed-valence dima nganese complexes and proteins is presented, based on the theory of Sa ge et al. (J. Am. Chem,Soc. 1989, 111, 7239-7247),which overcomes limi tations inherent in the theory of strongly coupled ions. This enables explanation of ''anomalous'' spectral parameters and extraction of acc urate g tensors and Mn-55 magnetic hyperfine tensors from which the sp atial distribution of the unpaired spin density, the electronic config uration, and ligand field parameters have been obtained, This is used to analyze highly accurate simulations of the EPR spectra, obtained by least-squares fits of two mixed valence oxidation states, from a seri es of dimanganese(II,III) and dimanganese(III,IV) complexes and from t he dimanganese catalase enzyme, MnCat(II,III) and MnCat(III,IV), from Thermus thermophilus. The sign of the Mn-55 dipolar hyperfine anisotro py (Delta a) reveals that the valence orbital configuration of the Mn( III) ion in MnCat(III,IV) and all dimanganese(III,IV) complexes posses sing sterically unconstrained bis(mu-oxo) bridges is d(pi)(3)(d(22))(1 ) with the antibonding d(22) electron oriented perpendicular to the pl ane of the Mn-2(mu-O)(2) rhombus. This accounts for the strong Mn-O bo nding and slow ligand exchange kinetics widely observed. The asymmetry of the spin density of Mn(III) increases substantially from Delta a/a (iso) = 0.27 in MnCat(III,IV) to 0.46 in MnCat(II,III), reflecting a c hange in manganese coordination. Comparison with model complexes sugge st this may be due to protonation and opening of the (mu-O)(2) bridge upon reduction to yield a single mu-OH bridge. The presence of strong Mn-O bonding in an unreactive (mu-O)(2) core of MnCat(III,IV) offers a plausible explanation for the 10(12) slower kinetics of peroxide dism utation compared to what is observed for the physiologically important oxidation state MnCat(II,II). For the dimanganese(II,III) oxidation s tate, the theory also provides the first explanation for the anomalous ly large (similar to 30%) Mn-55(II) hyperfine anisotropy in terms of a dmiring of the S = 3/2 excited state into the ground state (S = 1/2) v ia the zero-freld splitting interaction of Mn(III). This ''transferred '' anisotropy obscures the otherwise typical isotropic high-spin 3d(5) orbital configuration of Mn(II). An estimate of the ratio of the zero -field splitting to the Heisenberg exchange interaction (D/J) is obtai ned. The theory also explains the unusuarl 12-line EPR spectrum for a weakly coupled dimanganese(III,IV) complex (Larson et al. J. Am. Chem. Sec. 1992, 114, 6263-6265), in contrast to the typical 16-line ''mult iline'' spectra seen in strongly coupled dimanganese(III,IV) complexes . The theory shows this is due to a weak J = -10 cm(-1) which results in a D/J ratio approaching unity and not to unusual intrinsic magnetic hyperfine parameters of the Mn ions.