Redox Isomerism in the S₃ State of the Oxygen‐Evolving Complex Resolved by Coupled Cluster Theory

Abstract

The electronic and geometric structures of the water-oxidizing complex of photosystem II in the steps of the catalytic cycle that precede dioxygen evolution remain hotly debated. Recent structural and spectroscopic investigations support contradictory redox formulations for the active-site Mn 4 CaO x cofactor in the final metastable S 3 state. These range from the widely accepted Mn IV 4 oxo-hydroxo model, which presumes that OÀ O bond formation occurs in the ultimate transient intermediate (S 4 ) of the catalytic cycle, to a Mn III 2 Mn IV 2 peroxo model representative of the contrasting "early-onset" OÀ O bond formation hypothesis. Density functional theory energetics of suggested S 3 redox isomers are inconclusive because of extreme functional dependence.Here, we use the power of the domain-based local pair natural orbital approach to coupled cluster theory, DLPNO-CCSD(T), to present the first correlated wave function theory calculations of relative stabilities for distinct redox-isomeric forms of the S 3 state. Our results enabled us to evaluate conflicting models for the S 3 state of the oxygen-evolving complex (OEC) and to quantify the accuracy of lower-level theoretical approaches. Our assessment of the relevance of distinct redox-isomeric forms for the mechanism of biological water oxidation strongly disfavors the scenario of early-onset OÀ O formation advanced by literal interpretations of certain crystallographic models. This work serves as a case study in the application of modern coupled cluster implementations to redox isomerism problems in oligonuclear transition metal systems.

The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

“…Nevertheless, a very recent theoretical study considers a peroxidic intermediate in the S 3 state as unlikely. 96 By contrast, our substrate water exchange data are inconsistent with nucleophilic attack mechanisms between W3 and W2, 51,97–99 and geminal coupling between W2 and O5 at Mn4 (ref. 30, 100 ) (for details see ESI Text 4 and Fig.…”

Ab Initio Methods in First‐Row Transition Metal Chemistry

“…Thus, different extrapolations of local parameters have been proposed. For example, one can extrapolate to the complete PNO space using the equation E ∞ = E x + F ⋅ ( E y − E x ), where E x and E y are the correlation energies calculated with T CutPNO =10 − x and 10 − y , E ∞ is the extrapolated correlation energy at the PNO space limit, and F is a constant with the recommended value of 1.5 [68–70] …”

“…[225] Drouso and Pantazis used DLPNO-CCSD(T) to calculate the relative energy of two isomers of S 3 : the S = 6 Mn IV 4 oxo-hydroxo model and the S = 7 Mn III 2 Mn IV 2 peroxo model. [70] Yamaguchi et al introduced a series of studies on Mn 4 CaO 5 with DLPNO-CCSD(T): ten S 0 structures, [226] twelve S = 7 S 1 structures, [227] and various S 2 structures with S = 13/2, 5/2, 1/ 2. [228,229] The energy spectrum of [4FeÀ 4S] was first explored with DMRG by Sharma et al, [230] followed by two appers of Li Manni et al using FCIQMC.…”

Addressing the System-Size Dependence of the Local Approximation Error in Coupled-Cluster Calculations

“…For example, CPS(6/7) extrapolation yields errors in relative energies that are typically less than 0.3 kcal/mol in comparison to canonical CCSD(T) for the most challenging reactions of the GMTKN55 superset, 20 as shown in ref ( 45 ), as well as on many other molecular systems. 46 − 48 In particular, the accurate quantification of NCI energies 20 , 49 − 64 is a very hot topic of research. On the most popular benchmark set of NCIs (S66), 65 − 67 CPS(6/7) provides a mean absolute error (MAE) of only 0.03 kcal/mol at the complete basis set (CBS) limit relative to the SILVER 61 reference values.…”