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

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.

Mononuclear Non-Heme Manganese-Catalyzed Enantioselective cis-Dihydroxylation of Alkenes Modeling Rieske Dioxygenases

“…Indeed, Mn–O bonding in 3 IC2 (Mn–O distance: 1.69 Å) is much stronger than that in 5 IC2 (Mn–O distance: 1.80 Å). Such a finding is reminiscent of the stability of Mn­(IV)-oxyl species in Photosystem II (PSII) . Therefore, the generation of the HO–Mn V O species involves a typical two-state reactivity .…”

“…Such a finding is reminiscent of the stability of Mn(IV)-oxyl species in Photosystem II (PSII). 40 Therefore, the generation of the HO−Mn V �O species involves a typical two-state reactivity. 41 In comparison, we also investigated the non-water-assisted pathway for the generation of HO−Mn V �O species from the Mn III −OOH precursor (Figure S9), but the reaction requires a high barrier of 31.4 kcal mol −1 , which is highly unfavorable kinetically (Figure S9).…”

Mechanisms of Mn(V)‐Oxo to Mn(IV)‐Oxyl Conversion: From Closed‐Cubane Photosystem II to Mn(V) Catalysts and the Role of the Entering Ligands

“…First and foremost, we want to emphasise that the primary goal of this work is to investigate the mechanism for the transition from a Mn(V)‐oxo complex to a Mn(IV)‐oxyl complex and the role of water (or an entering ligand) in promoting this critical transformation. Consequently, this work does not aim to explore the detailed mechanism of O 2 evolution from the S 4 state $${{{\bf S}}_{4}^{{\bf B},{\bf U}}{\rm \ }}$$ as this process has recently been examined by various research groups [8,9b,13] . As demonstrated in the subsequent sections, the transition from a Mn(V)‐oxo complex to a Mn(IV)‐oxyl species is primarily influenced by the electronic properties of the core structure of the OEC complex.…”

Evolution in the Design of Water Oxidation Catalysts with Transition-Metals: A Perspective on Biological, Molecular, Supramolecular, and Hybrid Approaches

“…The OEC consists of an oxo-bridged tetranuclear manganese–calcium cluster (Mn 4 CaO 5 ) at its active site. Complementary spectroscopic and computational techniques have unearthed in-depth insights on this riveting mechanism, that leads to a four-electron redox chemistry of two water molecules in the OEC, encompassing five sequential intermediate states in the Kok cycle, resulting in the crucial O–O bond formation (see Figure , vide infra). − X-ray diffraction techniques with free-electron lasers (XFEL) and other advanced spectroscopic approaches have contributed immensely to elaborate the geometric and electronic templates that are involved in the plausible substrate water coupling and release of dioxygen, − providing a solid foundation for future functional studies. , Thus, the biological photosynthetic complex serves as a natural platform which could be probed to provide useful guidelines in the quest for light-driven artificial water splitting catalyst (Scheme ). ,− …”