Catalytic Cooperativity of Mono-Manganese and Tri-Manganese Clusters for Water-Splitting and Oxygen-Evolving Reaction in Photosystem II: Chemical Mechanistic Insight

Abstract

Applying the UDFT/B3LYP/(lacvp**, lacv3p**) geometry optimization method together with a Poisson-Boltsman equation solver in the e = 4 dielectric medium to a version-upped “truncated-OEC-cluster” model of MT-type, we found that (1) Upon the S_i-state transitions (I = 0 — 4) in a cyclic change of the most-stable tautomer(s), a proton release pattern of 1:0:1:2 has been derived with use of calculated exothermic vs endothermic energies, to yield the oxidation states: S₀Mn_a ^III; Mn_b ^III, Mn_c ^III, Mn_d ^IV, S₁Mn_a ^III; Mn_b ^IV, Mn_c ^III, Mn_d ^IV, S₂ ⁺Mn_a ^IV; Mn_b ^IV, Mn_c ^III, Mn_d ^IV, S₃ ⁺Mn_a ^IV; Mn_b ^IV, Mn_c ^IV, Mn_d ^IV and S_4aMn_a ^IV; Mn_b ^IV, Mn_c ^IV, Mn_d ^IV, (2) The redox potential for the last S₃/S_4a ⁺ oxidation step has been evaluated to be ca.1.07 V, a significantly-reduced value due to the H-bonding network between Y_Z, H190 and C_a ²⁺-binding site in the Mn₄Ca cluster, (3) The S_4a-intermediate contains the catalytic Mn_a ^IV ion binding two adjoining substrate derivatives, a hydroxyl anion (W1 = HO⁻) and an oxo radical (W2 = O^−·), and (4) The O-O bond formation is thermally induceable by a proton-coupled electron transfer (PCET) via a transition state with an activation energy of ca. 11.2 kcal/mol and a small exothermicity of ca. −4.5 kcal/mol, to yield a side-on superoxo anion radial bound to the Mn_a ^III ion in the second intermediate, formulated as S_4bMn_a ^III:O2^−·(W1 = W2); Mn_b ^IV, Mn_c ^III, Mn_d ^IV, where the third Mn_c ^III ion is in a low-spin state of S _c=1.