O–O Bond Formation and Oxygen Release in Photosystem II Are Enhanced by Spin-Exchange and Synergetic Coordination Interactions
Xitong Song, Binju Wang
Abstract
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.