O-O Bond Formation and Oxygen Release in Photosystem II Are Enhanced by Spin-Exchange and Synergetic Coordination Interactions.

The photosystem II (PSII)-catalyzed water oxidation is crucial for maintaining life on earth. Despite the extensive experimental and computational research that has been conducted over the past two decades, the mechanisms of O-O bond formation and oxygen release during the S 3 ∼ S 0 stage remain disputed. While the oxo-oxyl radical coupling mechanism in the "open-cubane" S 4 state is widely proposed, recent studies have suggested that O-O bond formation may occur from either the high-spin water-unbound S 4 state or the "closed-cubane" S 4 state. To gauge the various mechanisms of O-O bond formation proposed recently, the comprehensive QM/MM and QM calculations have been performed. Our studies show that both the nucleophilic O-O coupling from the Mn 4 site of the high-spin water-unbound S 4 state and the O 5 -O 6 or O 5 -O W2 coupling from the "closed-cubane" S 4 state are unfavorable kinetically and thermodynamically. Instead, the QM/MM studies clearly favor the oxyl-oxo radical coupling mechanism in the "open-cubane" S 4 state. Furthermore, our comparative research reveals that both the O-O bond formation and O 2 release are dictated by (a) the exchange-enhanced reactivity and (b) the synergistic coordination interactions from the Mn 1 , Mn 3 , and Ca sites, which partially explains why nature has evolved the oxygen-evolving complex cluster for the water oxidation.