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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 O-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" O-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 O-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., (© 2021 The Authors. Chemistry - A European Journal published by Wiley-VCH GmbH.)

The tetramanganese-calcium cluster of the oxygen-evolving complex of photosystem II adopts electronically and magnetically distinct but interconvertible valence isomeric forms in its first light-driven oxidized catalytic state, S 2 . This bistability is implicated in gating the final catalytic states preceding O-O bond formation, but it is unknown how the biological system enables its emergence and controls its effect. Here we show that the Mn 4 CaO 5 cluster in the resting (dark-stable) S 1 state adopts orientational Jahn-Teller isomeric forms arising from a directional change in electronic configuration of the "dangler" Mn III ion. The isomers are consistent with available structural data and explain previously unresolved electron paramagnetic resonance spectroscopic observations on the S 1 state. This unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S 2 state, establishing a functional role of orientational Jahn-Teller isomerism unprecedented in biological or artificial catalysis., (© 2021 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH.)

The investigation of water oxidation in photosynthesis has remained a central topic in biochemical research for the last few decades due to the importance of this catalytic process for technological applications. Significant progress has been made following the 2011 report of a high-resolution X-ray crystallographic structure resolving the site of catalysis, a protein-bound Mn 4 CaO x complex, which passes through ≥5 intermediate states in the water-splitting cycle. Spectroscopic techniques complemented by quantum chemical calculations aided in understanding the electronic structure of the cofactor in all (detectable) states of the enzymatic process. Together with isotope labeling, these techniques also revealed the binding of the two substrate water molecules to the cluster. These results are described in the context of recent progress using X-ray crystallography with free-electron lasers on these intermediates. The data are instrumental for developing a model for the biological water oxidation cycle.

Heterogeneity in intermediate catalytic states of the oxygen-evolving complex (OEC) of Photosystem II is known from a wide range of experimental and theoretical data, but its potential implications for the mechanism of water oxidation remain unexplored. We delineate the consequences of structural heterogeneity for the final step of the catalytic cycle by tracing the evolution of three spectroscopically relevant and structurally distinct components of the last metastable S 3 state to the transient O 2 -evolving S 4 state of the OEC. Using quantum chemical calculations, we show that each S 3 isomer leads to a different electronic structure formulation for the active S 4 state. Crucially, in addition to previously hypothesized Mn(IV)-oxyl species, we establish for the first time, how a genuine Mn(V)-oxo can be obtained in the catalytically active S 4 state: this takes the form of a five-coordinate and locally high-spin (S Mn  = 1) Mn(V) site. This formulation for the S 4 state evolves naturally from a preceding S 3 -state structural intermediate that contains a quasi-trigonal-bipyramidal Mn(IV) ion. The results strongly suggest that water binding in the S 3 state is not prerequisite for reaching the oxygen-evolving S 4 state of the complex, supporting the notion that both substrates are preloaded at the beginning of the catalytic cycle. This scenario allows true four-electron metal-centered hole accumulation to precede OO bond formation and hence the latter can proceed via a genuine even-electron mechanism. This can occur as intramolecular nucleophilic coupling of two oxo units synchronously with the binding of a water substrate for the next catalytic cycle., (Copyright © 2019 Elsevier Inc. All rights reserved.)

The accurate description of magnetic level energetics in oligonuclear exchange-coupled transition-metal complexes remains a formidable challenge for quantum chemistry. The density matrix renormalization group (DMRG) brings such systems for the first time easily within reach of multireference wave function methods by enabling the use of unprecedentedly large active spaces. But does this guarantee systematic improvement in predictive ability and, if so, under which conditions? We identify operational parameters in the use of DMRG using as a test system an experimentally characterized mixed-valence bis-μ-oxo/μ-acetato Mn(III,IV) dimer, a model for the oxygen-evolving complex of photosystem II. A complete active space of all metal 3d and bridge 2p orbitals proved to be the smallest meaningful starting point; this is readily accessible with DMRG and greatly improves on the unrealistic metal-only configuration interaction or complete active space self-consistent field (CASSCF) values. Orbital optimization is critical for stabilizing the antiferromagnetic state, while a state-averaged approach over all spin states involved is required to avoid artificial deviations from isotropic behavior that are associated with state-specific calculations. Selective inclusion of localized orbital subspaces enables probing the relative contributions of different ligands and distinct superexchange pathways. Overall, however, full-valence DMRG-CASSCF calculations fall short of providing a quantitative description of the exchange coupling owing to insufficient recovery of dynamic correlation. Quantitatively accurate results can be achieved through a DMRG implementation of second order N-electron valence perturbation theory (NEVPT2) in conjunction with a full-valence metal and ligand active space. Perspectives for future applications of DMRG-CASSCF/NEVPT2 to exchange coupling in oligonuclear clusters are discussed.

Multifrequency pulsed EPR data are reported for a series of oxygen bridged (μ-oxo/μ-hydroxo) bimetallic manganese complexes where the oxygen is labeled with the magnetically active isotope (17)O (I = 5/2). Two synthetic complexes and two biological metallocofactors are examined: a planar bis-μ-oxo bridged complex and a bent, bis-μ-oxo-μ-carboxylato bridge complex; the dimanganese catalase, which catalyzes the dismutation of H2O2 to H2O and O2, and the recently identified manganese/iron cofactor of the R2lox protein, a homologue of the small subunit of the ribonuclotide reductase enzyme (class 1c). High field (W-band) hyperfine EPR spectroscopies are demonstrated to be ideal methods to characterize the (17)O magnetic interactions, allowing a magnetic fingerprint for the bridging oxygen ligand to be developed. It is shown that the μ-oxo bridge motif displays a small positive isotropic hyperfine coupling constant of about +5 to +7 MHz and an anisotropic/dipolar coupling of -9 MHz. In addition, protonation of the bridge is correlated with an increase of the hyperfine coupling constant. Broken symmetry density functional theory is evaluated as a predictive tool for estimating hyperfine coupling of bridging species. Experimental and theoretical results provide a framework for the characterization of the oxygen bridge in Mn metallocofactor systems, including the water oxidizing cofactor of photosystem II, allowing the substrate/solvent interface to be examined throughout its catalytic cycle.

The assignment of the two substrate water sites of the tetra-manganese penta-oxygen calcium (Mn4O5Ca) cluster of photosystem II is essential for the elucidation of the mechanism of biological O-O bond formation and the subsequent design of bio-inspired water-splitting catalysts. We recently demonstrated using pulsed EPR spectroscopy that one of the five oxygen bridges (μ-oxo) exchanges unusually rapidly with bulk water and is thus a likely candidate for one of the substrates. Ammonia, a water analog, was previously shown to bind to the Mn4O5Ca cluster, potentially displacing a water/substrate ligand [Britt RD, et al. (1989) J Am Chem Soc 111(10):3522-3532]. Here we show by a combination of EPR and time-resolved membrane inlet mass spectrometry that the binding of ammonia perturbs the exchangeable μ-oxo bridge without drastically altering the binding/exchange kinetics of the two substrates. In combination with broken-symmetry density functional theory, our results show that (i) the exchangable μ-oxo bridge is O5 {using the labeling of the current crystal structure [Umena Y, et al. (2011) Nature 473(7345):55-60]}; (ii) ammonia displaces a water ligand to the outer manganese (MnA4-W1); and (iii) as W1 is trans to O5, ammonia binding elongates the MnA4-O5 bond, leading to the perturbation of the μ-oxo bridge resonance and to a small change in the water exchange rates. These experimental results support O-O bond formation between O5 and possibly an oxyl radical as proposed by Siegbahn and exclude W1 as the second substrate water.

A systematic study of the magnetic coupling in homovalent (III-III and IV-IV) and heterovalent (III-IV) manganese dimers as a function of the chemical identity and coordination mode of the bridging ligands is carried out with the aim of establishing a reference library of magnetostructural correlations. Emphasis is placed on rationalising the results through analysis of the superexchange pathways in terms of corresponding orbitals. Additionally, the influence of specific structural distortions on magnetic properties is explored. Consistent with chemical intuition and decades of experience, oxo bridges are shown to be efficient mediators of superexchange, primarily through pi-type pathways, whereas the introduction of bridging carboxylates inhibits the magnetic coupling of the metal centres by introducing structural distortions in the core and by reducing the antiferromagnetic contribution to the exchange. Protonation of oxo bridges is shown to induce a predictably systematic reduction in the magnitude of antiferromagnetic coupling by switching off the dominant antiferromagnetic exchange pathways. In the case of weakly coupled dimers, this can even induce a reversal of the coupling from antiferromagnetic to ferromagnetic.

Exchange coupling parameters and isotropic (55)Mn hyperfine couplings of fourteen mixed-valence Mn(III)-Mn(IV) dimers are determined using broken-symmetry density functional theory (DFT) and spin projection techniques. A systematic evaluation of density functional approaches shows that the TPSSh functional yields the best exchange coupling constants among all investigated methods, with deviations from experiment of the order of approximately 10-15%. For the prediction of (55)Mn hyperfine couplings the deficiencies of DFT in the description of core-level spin-polarization and the neglect of scalar relativistic effects lead to systematic deviations between theory and experiment that can be compensated through the use of a universal scaling factor. We determine this scaling factor to be 1.49 and demonstrate that the (55)Mn hyperfine couplings in mixed-valence Mn(III,IV) dimers can be successfully and systematically predicted with the TPSSh functional and the proposed spin projection techniques. The dependence of isotropic (55)Mn hyperfine couplings on the Mn(III) zero-field splitting values is studied in detail using a dimer for which the strong exchange approximation breaks down. In this case we apply a rigorous form of our spin projection technique that incorporates zero-field splitting contributions to the site spin expectation values. These results form the basis for future studies that aim at deducing unknown structures on the basis of computed spectroscopic parameters.

The reliable correlation of structural features and magnetic or spectroscopic properties of oligonuclear transition-metal complexes is a critical requirement both for research into innovative magnetic materials and for elucidating the structure and function of many metalloenzymes. We have developed a novel method that for the first time enables the extraction of hyperfine coupling constants (HFCs) from broken-symmetry density functional theory (BS-DFT) calculations on clusters. Using the geometry-optimized tetranuclear manganese complex [Mn(4)O(6)(bpy)(6)](4+/3+) as a model, we first examine in detail the calculation of exchange coupling constants J through the BS-DFT approach. Complications arising from the indeterminacy of experimentally fitted J constants are identified and analyzed. It is found that only the energy levels derived from Hamiltonian diagonalization are a physically meaningful basis for comparing theory and experiment. Subsequently, the proposed theoretical scheme is applied to the calculation of (55)Mn HFCs of the Mn(III,IV,IV,IV) state of the complex, which is similar to the S(2) state of the oxygen-evolving complex (OEC) in photosystem II of oxygenic photosynthesis. The new approach performs reliably and accurately, and yields calculated HFCs that can be directly compared with experimental data. Finally, we carefully examine the dependence of HFC on the J value and draw attention to the sensitivity of the calculated values to the exchange coupling parameters. The proposed strategy extends naturally to hetero-oligonuclear clusters of arbitrary shape and nuclearity, and hence is of general validity and usefulness in the study of magnetic metal clusters. The successful application of the new approach presented here is a first step in the effort to establish correlations between the available spectroscopic information and the structural features of complex metalloenzymes like OEC.