Theory of Chemical Bonds in Metalloenzymes. XV. Local Singlet and Triplet Diradical Mechanisms for Radical Coupling Reactions in the Oxygen Evolution Complex

Reaction mechanisms of oxygen evolution in native and artificial photosynthesis IT (PSII) systems have been investigated on the theoretical grounds, together with experimental results. First of all, our previous broken-symmetry (BS) molecular orbitals (MO) calculations are reviewed to elucidate the instability of the d pi-p pi bond in high-valent (HIV) Mn(X)=O systems and the d pi-p pi-d pi bond in HV Mn=O=Mn systems. The triplet instability of these bonds entails strong or intermediate diradical characters: center dot Mn(IV)=O center dot and center dot Mn-O-Mn center dot; the BS MO resulted from strong electron correlation, leading to the concept of electron localizations and local spins. The BS computations have furthermore revealed guiding principles for derivation of selection rules for radical reactions of local spins. As a continuation of these theoretical results, the BS MO interaction diagrams for oxygen-radical coupling reactions in the oxygen evolution complex (OEC) in the PSII have been depicted to reveal scope and applicability of local singlet diradical (LSD) and local triplet diradical (LTD) mechanisms that have been successfully utilized for theoretical understanding of oxygenation reactions mechanisms by p450 and methane monooxygenase (MMO). The manganese-oxide cluster models examined are London, Berlin, and Berkeley models of CaMn4O4 and related clusters Mn4O4 and Mn3Ca. The BS MO interaction diagrams have revealed the LSD and/or LTD mechanisms for generation of molecular oxygen in the total low-, intermediate and high-spin states of these clusters. The spin alignments are found directly corresponding to the spin-coupling mechanisms of oxygen-radical sites in these clusters. The BS UB3LYP calculations of the clusters have been performed to confirm the comprehensive guiding principles for oxygen evolution; charge and spin densities by BS UB3LYP are utilized for elucidation and confirmation of the LSD and LTD mechanisms. Applicability of the proposed selection rules are examined in comparison with a lot of accumulated experimental and theoretical results for oxygen evolution reactions in native and artificial PSII systems. (C) 2010 Wiley Periodicals, Inc. Int J Quantum Chem 110: 3101-3128, 2010