Theory of chemical bonds in metalloenzymes. XV. Local singlet and triplet diradical mechanisms for radical coupling reactions in the oxygen evolution complex

Abstract

Reaction mechanisms of oxygen evolution in native and artificial photosynthesis II (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 dp-pp bond in high-valent (HV) Mn(X)¼ ¼O systems and the dp-pp-dp bond in HV Mn¼ ¼O¼ ¼Mn systems. The triplet instability of these bonds entails strong or intermediate diradical characters: Mn(IV)¼ ¼O and MnAOAMn; 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 CaMn 4 O 4 and related clusters Mn 4 O 4 and Mn 3 Ca. The BS MO interaction diagrams have revealed the LSD and/or LTD mechanisms for generation of molecular oxygen in the total low-, intermediate and highspin 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.

Similarities of artificial photosystems by ruthenium oxo complexes and native water splitting systems

“…Moreover, BS solutions for MnðVÞ═O indicate continuous variation from the nucleophilic MnðVÞ═O 2− oxygen to electrophilic oxygen MnðIIIÞ═O 0 through •MnðIVÞ═O•, depending on electron donating ability of coordination ligands. In fact, oxyl radical character is computationally detected even in the prophyrine MnðVÞ═O complex (44). We have thoroughly examined the radical-coupling (RC) mechanism for the O─O bond formation process for the CaMn 4 O 5 cluster (3) in hydrophobic conditions (gas phase) like in the case of the Tanaka catalysts (Fig.…”

Theory of chemical bonds in metalloenzymes. XVII. Symmetry breaking in manganese cluster structures and chameleonic mechanisms for the OO bond formation of water splitting reaction

“…However, multicenter Mn complexes are necessary for the next step: namely facile deprotonation of MnOOH (or MnHOOH) to generate triplet molecular oxygen (;OAO;). As shown previously [26,48], the ferromagnetic exchange- [11][12][13][14][15][16][17][18]. As mentioned above, Dismukes [12] has elucidated that cuboid Mn 4 O 4 oxides (Ia) depicted in Figure 7 undergoes the OAO bond formation via the radical-coupling mechanism (see also A in Scheme 2).…”

“…The key points are the OAO bond formation and oxygen evolution in water splitting reaction. As shown in part XV [26], the homolytic diradical mechanism is conceivable if one of oxygen atom in the Ca(II)Mn 4 O 4 skeleton of IIIa-VIa is involved in the OAO bond formation with the dangling spin-polarized Mn(IV)¼ ¼O. Siegbahn [53][54][55] has performed many UB3LYP calculations for this type of the OAO bond formation starting from IIIa.…”

“…This means that multinuclear manganese complexes are crucial for a smooth OAO bond formation without a spin cross over. As shown previously, several guiding principles for structure and reactivity of manganese oxides have been obtained by the previous BS DFT calculations of these species [26,34,[41][42][43]. These principles (A-F) summarized in Supporting Information can be used for the water splitting reaction in the OEC.…”

“…Thus, symmetry and broken symmetry play an important role for characterization of cluster structures of multinuclear iron-sulfur complexes in chemistry and biology. These are closely related to homolytic and heterolytic bond cleavages (or formations) in chemical reaction as discussed previously [3,4,[22][23][24][25]26]. SCHEME 1.…”