A Theoretical Study of the Recently Suggested Mn^VII Mechanism for O–O Bond Formation in Photosystem II

Abstract

The mechanism for water oxidation in photosystem II has been a major topic for several decades. The active catalyst has four manganese atoms connected by bridging oxo bonds, in a complex termed the oxygen-evolving complex (OEC), which also includes a calcium atom. The O–O bond of oxygen is formed after absorption of four photons in a state of the OEC termed S 4 . There has been essential consensus that in the S 4 state, all manganese atoms are in the Mn(IV) oxidation state. However, recently there has been a suggestion that one of the atoms is in the Mn(VII) state. In the present computational study, the feasibility of that proposal has been investigated. It is here shown that the mechanism involving Mn(VII) has a much higher barrier for forming O 2 than the previous proposal with four Mn(IV) atoms.

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

“…Contrasting mechanistic studies by Zhang and Sun suggests the formation of a Mn VII -dioxo intermediate as the dangling metal site for water oxidation in the S 4 state of the Kok cycle . Extensive DFT studies by Li and others reveal that the existence of a Mn VII O moiety is very unlikely, due to the large energetic cost involved in transition from S 3 to S 4 (+33.8 kcal/mol at B3LYP/LACVP) as compared to the insignificant endergonicity of the analogous transformation with all Mn IV ions (+5.7 kcal/mol) . In a latest theoretical study, Messinger, Sun, and others , indicate that unlike cyanobacterial photosystems, the S 3 state of higher plants are devoid of the additional Mn-bound oxygenic ligand necessary for a “radical coupling” through the Mn IV –O • (oxyl) moiety in an open-cubane cluster, as shown in Figure (bottom).…”

“…18 Extensive DFT studies by Li and others reveal that the existence of a Mn VII �O moiety is very unlikely, due to the large energetic cost involved in transition from S 3 to S 4 (+33.8 kcal/mol at B3LYP/LACVP) as compared to the insignificant endergonicity of the analogous transformation with all Mn IV ions (+5.7 kcal/mol). 102 In a latest theoretical study, Messinger, Sun, and others 103,104 indicate that unlike cyanobacterial photosystems, the S 3 state of higher plants are devoid of the additional Mn-bound oxygenic ligand necessary for a "radical coupling" through the Mn IV −O • (oxyl) moiety in an open-cubane cluster, as shown in Figure 4 (bottom). The authors further propose that the S 3 state in higher plants undergo considerable structural modifications on binding of water and attain a specific conformation that enables the dangling Mn V �O exhibit a "nucleophilic oxo-oxo coupling" with a μ 3 -oxo group of the closed-cubane motif in the resulting unbound S 4 state (Scheme 2).…”

Mimicking the Oxygen-Evolving Center in Photosynthesis

“…The third model ( Figure 3C ) was proposed by Sun group ( Zhang and Sun, 2019a ), in which one Mn VII ion was suggested to be involved in the S 4 state. This mechanism has been recently evaluated by a computational study that shows that the formation of the Mn VII requires a much higher barrier for forming O 2 than the earlier proposals with four Mn IV atoms ( Li et al, 2020a ). The fourth model, originally proposed by Siegbahn ( Siegbahn, 2013 ), and then other groups ( Pecoraro et al, 1998 ; Cox et al, 2020 ), is where the μ 4 -oxide bridge (O5) and the newly inserted water (O 6 ) are considered to serve as the oxygen source for the O=O bond ( Figure 3D ).…”

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

“…For the last transition (S 3 → S 0 ), which is the focus of our study, the reaction involves the O–O bond formation and O 2 release from the transient S 4 state. In spite of extensive studies, the mechanism of O–O bond formation during the S 3 → S 4 → S 0 transition remains elusive. ,,,− As the transient S 4 structure lacks the experimental characterization, extensive computational studies have focused on the O–O bond formation and O 2 release mechanism during S 3 → S 0 . − Currently, there are two general mechanisms for O–O bond formation, which are displayed in Scheme . One is the nucleophilic attack mechanism, ,− and the other is the oxo-oxyl radical coupling mechanism, which was first suggested by Siegbahn in 2006 .…”

“…70 Though many types of other nucleophilic attack mechanisms involving different sources of the nucleophilic oxygen (e.g., W 1 −W 4 , as well as O 4 , O 5 and O 6 as shown in Figure 1d) have been proposed by different groups, none of these mechanisms has been sufficiently supported by computational studies. 57,58,70 Interestingly, the nucleophilic attack mechanism has been supported in synthetic water-splitting systems, 76,77 suggesting that the catalysis of PSII is different from the one going on in synthetic model systems.…”