Merging Structural Information from X‑ray Crystallography, Quantum Chemistry, and EXAFS Spectra: The Oxygen-Evolving Complex in PSII

Structural data of the oxygen-evolving complex (OEC) in photosystem II (PSII) determined by X-ray crystallography, quantum chemistry (QC), and extended X-ray absorption fine structure (EXAFS) analyses are presently inconsistent. Therefore, a detailed study of what information can be gained about the OEC through a comparison of QC and crystallographic structure information combined with the information from range-extended EXAFS spectra was undertaken. An analysis for determining the precision of the atomic coordinates of the OEC by QC is carried out. OEC model structures based on crystallographic data that are obtained by QC from different research groups are compared with one another and with structures obtained by high-resolution crystallography. The theory of EXAFS spectra is summarized, and the application of EXAFS spectra to the experimental determination of the structure of the OEC is detailed. We discriminate three types of parameters entering the formula for the EXAFS spectrum: (1) model-independent, predefined, and fixed; (2) model-dependent that can be computed or adjusted; and (3) model-dependent that must be adjusted. The information content of EXAFS spectra is estimated and is related to the precision of atomic coordinates and resolution power to discriminate different atom-pair distances of the OEC. It is demonstrated how a precise adjustment of atomic coordinates can yield a nearly perfect representation of the experimental OEC EXAFS spectrum, but at the expense of overfitting and losing the knowledge of the initial OEC model structure. Introducing a novel type of penalty function, it is shown that moderate adjustment of atomic coordinates to the EXAFS spectrum limited by constraints avoids overfitting and can be used to validate different OEC model structures. This technique is used to identify the OEC model structures whose computed OEC EXAFS spectra agree best with the measured spectrum. In this way, the most likely S-state and protonation pattern of the OEC for the most recent high-resolution crystal structure of PSII are determined. We find that the X-ray free-electron laser (XFEL) structure is indeed not significantly affected by exposure to XFEL pulses and thus results in a radiation-damage-free model of the OEC

Electronic Structure of an [FeFe] Hydrogenase Model Complex in Solution Revealed by X‑ray Absorption Spectroscopy Using Narrow-Band Emission Detection

High-resolution X-ray absorption spectroscopy with narrow-band X-ray emission detection, supported by density functional theory calculations (XAES-DFT), was used to study a model complex, ([Fe₂(μ-adt)­(CO)₄(PMe₃)₂] (<b>1</b>, adt = S–CH₂–(NCH₂Ph)–CH₂–S), of the [FeFe] hydrogenase active site. For <b>1</b> in powder material (<b>1</b>_powder), in MeCN solution (<b>1</b>′), and in its three protonated states (<b>1H</b>, <b>1Hy</b>, <b>1HHy</b>; <b>H</b> denotes protonation at the adt–N and <b>Hy</b> protonation of the Fe–Fe bond to form a bridging metal hydride), relations between the molecular structures and the electronic configurations were determined. EXAFS analysis and DFT geometry optimization suggested prevailing rotational isomers in MeCN, which were similar to the crystal structure or exhibited rotation of the (CO) ligands at Fe1 (<b>1</b>_CO, <b>1Hy</b>_CO) and in addition of the phenyl ring (<b>1H</b>_CO,Ph, <b>1HHy</b>_CO,Ph), leading to an elongated solvent-exposed Fe–Fe bond. Isomer formation, adt–N protonation, and hydride binding caused spectral changes of core-to-valence (pre-edge of the Fe K-shell absorption) and of valence-to-core (Kß^2,5 emission) electronic transitions, and of Kα RIXS data, which were quantitatively reproduced by DFT. The study reveals (1) the composition of molecular orbitals, for example, with dominant Fe-d character, showing variations in symmetry and apparent oxidation state at the two Fe ions and a drop in MO energies by ∼1 eV upon each protonation step, (2) the HOMO–LUMO energy gaps, of ∼2.3 eV for <b>1</b>_powder and ∼2.0 eV for <b>1</b>′, and (3) the splitting between iron d­(<i>z</i>²) and d­(<i>x</i>²–<i>y</i>²) levels of ∼0.5 eV for the nonhydride and ∼0.9 eV for the hydride states. Good correlations of reduction potentials to LUMO energies and oxidation potentials to HOMO energies were obtained. Two routes of facilitated bridging hydride binding thereby are suggested, involving ligand rotation at Fe1 for <b>1Hy</b>_CO or adt–N protonation for <b>1HHy</b>_CO,Ph. XAES-DFT thus enables verification of the effects of ligand substitutions in solution for guided improvement of [FeFe] catalysts

Site-Selective X-ray Spectroscopy on an Asymmetric Model Complex of the [FeFe] Hydrogenase Active Site

The active site for hydrogen production in [FeFe] hydrogenase comprises a diiron unit. Bioinorganic chemistry has modeled important features of this center, aiming at mechanistic understanding and the development of novel catalysts. However, new assays are required for analyzing the effects of ligand variations at the metal ions. By high-resolution X-ray absorption spectroscopy with narrow-band X-ray emission detection (XAS/XES = XAES) and density functional theory (DFT), we studied an asymmetrically coordinated [FeFe] model complex, [(CO)₃Fe^I1-(bdtCl₂)-Fe^I2­(CO)­(Ph₂P–CH₂–NCH₃–CH₂–PPh₂)] (<b>1</b>, bdt = benzene-1,2-dithiolate), in comparison to iron–carbonyl references. Kβ emission spectra (Kβ^1,3, Kβ′) revealed the absence of unpaired spins and the low-spin character for both Fe ions in <b>1</b>. In a series of low-spin iron compounds, the Kβ^1,3 energy did not reflect the formal iron oxidation state, but it decreases with increasing ligand field strength due to shorter iron-ligand bonds, following the spectrochemical series. The intensity of the valence-to-core transitions (Kβ^2,5) decreases for increasing Fe-ligand bond length, certain emission peaks allow counting of Fe-CO bonds, and even molecular orbitals (MOs) located on the metal-bridging bdt group of <b>1</b> contribute to the spectra. As deduced from 3d → 1s emission and 1s → 3d absorption spectra and supported by DFT, the HOMO–LUMO gap of <b>1</b> is about 2.8 eV. Kβ-detected XANES spectra in agreement with DFT revealed considerable electronic asymmetry in <b>1</b>; the energies and occupancies of Fe-d dominated MOs resemble a square-pyramidal Fe(0) for Fe1 and an octahedral Fe­(II) for Fe2. EXAFS spectra for various Kβ emission energies showed considerable site-selectivity; approximate structural parameters similar to the crystal structure could be determined for the two individual iron atoms of <b>1</b> in powder samples. These results suggest that metal site- and spin-selective XAES on [FeFe] hydrogenase protein and active site models may provide a powerful tool to study intermediates under reaction conditions

Room-Temperature Energy-Sampling Kβ X‑ray Emission Spectroscopy of the Mn₄Ca Complex of Photosynthesis Reveals Three Manganese-Centered Oxidation Steps and Suggests a Coordination Change Prior to O₂ Formation

In oxygenic photosynthesis, water is oxidized and dioxygen is produced at a Mn₄Ca complex bound to the proteins of photosystem II (PSII). Valence and coordination changes in its catalytic S-state cycle are of great interest. In room-temperature (in situ) experiments, time-resolved energy-sampling X-ray emission spectroscopy of the Mn Kβ_1,3 line after laser-flash excitation of PSII membrane particles was applied to characterize the redox transitions in the S-state cycle. The Kβ_1,3 line energies suggest a high-valence configuration of the Mn₄Ca complex with Mn­(III)₃Mn­(IV) in S₀, Mn­(III)₂Mn­(IV)₂ in S₁, Mn­(III)­Mn­(IV)₃ in S₂, and Mn­(IV)₄ in S₃ and, thus, manganese oxidation in each of the three accessible oxidizing transitions of the water-oxidizing complex. There are no indications of formation of a ligand radical, thus rendering partial water oxidation before reaching the S₄ state unlikely. The difference spectra of both manganese Kβ_1,3 emission and K-edge X-ray absorption display different shapes for Mn­(III) oxidation in the S₂ → S₃ transition when compared to Mn­(III) oxidation in the S₁ → S₂ transition. Comparison to spectra of manganese compounds with known structures and oxidation states and varying metal coordination environments suggests a change in the manganese ligand environment in the S₂ → S₃ transition, which could be oxidation of five-coordinated Mn­(III) to six-coordinated Mn­(IV). Conceivable options for the rearrangement of (substrate) water species and metal–ligand bonding patterns at the Mn₄Ca complex in the S₂ → S₃ transition are discussed

Kα X‑ray Emission Spectroscopy on the Photosynthetic Oxygen-Evolving Complex Supports Manganese Oxidation and Water Binding in the S₃ State

The unique manganese–calcium catalyst in photosystem II (PSII) is the natural paragon for efficient light-driven water oxidation to yield O₂. The oxygen-evolving complex (OEC) in the dark-stable state (S₁) comprises a Mn₄CaO₄ core with five metal-bound water species. Binding and modification of the water molecules that are substrates of the water-oxidation reaction is mechanistically crucial but controversially debated. Two recent crystal structures of the OEC in its highest oxidation state (S₃) show either a vacant Mn coordination site or a bound peroxide species. For purified PSII at room temperature, we collected Mn Kα X-ray emission spectra of the S₀, S₁, S₂, and S₃ intermediates in the OEC cycle, which were analyzed by comparison to synthetic Mn compounds, spectral simulations, and OEC models from density functional theory. Our results contrast both crystallographic structures. They indicate Mn oxidation in three S-transitions and suggest additional water binding at a previously open Mn coordination site. These findings exclude Mn reduction and render peroxide formation in S₃ unlikely

Behavior of the Ru-bda Water Oxidation Catalyst Covalently Anchored on Glassy Carbon Electrodes

Electrochemical reduction of the dizaonium complex, [Ru^II(bda)­(NO)­(N–N₂)₂]³⁺, <b>2</b>³⁺ (N–N₂²⁺ is 4-(pyridin-4-yl) benzenediazonium and bda^2– is [2,2′-bipyridine]-6,6′-dicarboxylate), in acetone produces the covalent grafting of this molecular complex onto glassy carbon (GC) electrodes. Multiple cycling voltammetric experiments on the GC electrode generates hybrid materials labeled as <b>GC-4</b>, with the corresponding Ru-aqua complex anchored on the graphite surface. <b>GC-4</b> has been characterized at pH = 7.0 by electrochemical techniques and X-ray absorption spectroscopy (XAS) and has been shown to act as an active catalyst for the oxidation of water to dioxygen. This new hybrid material has a lower catalytic performance than its counterpart in homogeneous phase and progressively decomposes to form <b>RuO₂</b> at the electrode surface. Nevertheless the resulting metal oxide attached at the GC electrode surface, <b>GC-RuO</b>_<b>2</b>, is a very fast and rugged heterogeneous water oxidation catalyst with TOF_is of 300 s^–1 and TONs > 45 000. The observed performance is comparable to the best electrocatalysts reported so far, at neutral pH

H/D Isotope Effects Reveal Factors Controlling Catalytic Activity in Co-Based Oxides for Water Oxidation

Understanding the mechanism for electrochemical water oxidation is important for the development of more efficient catalysts for artificial photosynthesis. A basic step is the proton-coupled electron transfer, which enables accumulation of oxidizing equivalents without buildup of a charge. We find that substituting deuterium for hydrogen resulted in an 87% decrease in the catalytic activity for water oxidation on Co-based amorphous-oxide catalysts at neutral pH, while ¹⁶O-to-¹⁸O substitution lead to a 10% decrease. In situ visible and quasi-in situ X-ray absorption spectroscopy reveal that the hydrogen-to-deuterium isotopic substitution induces an equilibrium isotope effect that shifts the oxidation potentials positively by approximately 60 mV for the proton coupled Co^II/III and Co^III/IV electron transfer processes. Time-resolved spectroelectrochemical measurements indicate the absence of a kinetic isotope effect, implying that the precatalytic proton-coupled electron transfer happens through a stepwise mechanism in which electron transfer is rate-determining. An observed correlation between Co oxidation states and catalytic current for both isotopic conditions indicates that the applied potential has no direct effect on the catalytic rate, which instead depends exponentially on the average Co oxidation state. These combined results provide evidence that neither proton nor electron transfer is involved in the catalytic rate-determining step. We propose a mechanism with an active species composed by two adjacent Co^IV atoms and a rate-determining step that involves oxygen–oxygen bond formation and compare it with models proposed in the literature

Role of decomposition products in the oxidation of cyclohexene using a manganese(III) complex

Metal complexes are extensively explored as catalysts for oxidation reactions; molecular-based mechanisms are usually proposed for such reactions. However, the roles of the decomposition products of these materials in the catalytic process have yet to be considered for these reactions. Herein, the cyclohexene oxidation in the presence of manganese(III) 5,10,15,20-tetra(4-pyridyl)-21H,23H-porphine chloride tetrakis(methochloride) (1) in a heterogeneous system via loading the complex on an SBA-15 substrate is performed as a study case. A molecular-based mechanism is usually suggested for such a metal complex. Herein, 1 was selected and investigated under the oxidation reaction by iodosylbenzene or (diacetoxyiodo)benzene (PhI(OAc)2). In addition to 1, at least one of the decomposition products of 1 formed during the oxidation reaction could be considered a candidate to catalyze the reaction. First-principles calculations show that Mn dissolution is energetically feasible in the presence of iodosylbenzene and trace amounts of water.</p