Experimental and Computational X-ray Emission Spectroscopy as a Direct Probe of Protonation States in Oxo-Bridged Mn^IV Dimers Relevant to Redox-Active Metalloproteins

Abstract

The protonation state of oxo-bridges in nature is of profound importance for a variety of enzymes, including the Mn4CaO5 cluster of Photosystem II and the Mn2O2 cluster in Mn catalase. A set of dinuclear bis-μ-oxo-bridged MnIV complexes in different protonation states was studied by Kβ emission spectroscopy to form the foundation for unraveling the protonation states in the native complex. The valence-to-core regions (valence-to-core XES) of the spectra show significant changes in intensity and peak position upon protonation. DFT calculations were performed to simulate the valence-to-core XES spectra and to assign the spectral features to specific transitions. The Kβ2,5 peaks arise primarily from the ligand-2p to Mn-1s transitions, with a characteristic low energy shoulder appearing upon oxo-bridge protonation. The satellite Kβ″ peak provides a more direct signature of the protonation state change, since the transitions originating from the 2s orbitals of protonated and unprotonated μ-oxo-bridges dominate this spectral region. The energies of the Kβ″ features differ by ~ 3 eV and thus are well resolved in the experimental spectra. Additionally, our work explores the chemical resolution limits of the method, namely, whether a mixed (μ-O)(μ-OH2) motif can be distinguished from a symmetric (μ-OH)2 one. The results reported here highlight the sensitivity of Kβ valence-to-core XES to single protonation state changes of bridging ligands, and form the basis for further studies of oxo-bridged polymetallic complexes and metallo-enzyme active sites. In a complementary paper, the results from X-ray absorption spectroscopy of the same MnIV-dimer series are discussed.

The Protonation States of Oxo-Bridged MnIV Dimers Resolved by Experimental and Computational Mn K Pre-Edge X-ray Absorption Spectroscopy

“…Nevertheless, the asymmetrically protonated form 3b was investigated computationally to explore the limits of structural differentiation of K pre-edge X-ray absorption spectroscopy (this work) and valence-to-core X-ray emission spectroscopy (Ref. 14). …”

“…In the following back-to-back studies, 14 we explore X-ray absorption (XAS) and X-ray emission spectroscopy (XES) as means to experimentally establish ligand protonation states. X-ray based methods have the advantage of being element selective and independent of metal spin state.…”

X-ray Absorption and Emission Study of Dioxygen Activation by a Small-Molecule Manganese Complex

“…52 VtC XES calculations were performed within a one-electron DFT model, and were corrected for spin–orbit coupling using the spin–orbit mean-field method 53 as described previously. 33,34,38 XAS calculations were performed using the B3LYP functional and the TD-DFT method employing the Tamm–Dancoff 54,55 and the RI chain of spheres (RIJCOSX) approximations. 56–58 Fragment analysis was performed with MOAnalyzer, 59 and transition difference densities for XAS calculations and canonical orbitals for electronic structure and XES calculations were visualized with UCSF Chimera.…”

A Practical Guide to High‐resolution X‐ray Spectroscopic Measurements and their Applications in Bioinorganic Chemistry

“…An important advantage over EXAFS is the ability of VtC XES to separate ligand contributions based on ionization energy. Hence C, N, and O, may be distinguished by VtC XES, as can individual protonation events . Moreover, insight into metal‐ligand bond lengths, and the activation of diatomic ligands (CO, N 2 , O 2 , or NO) may also be extracted from analysis of VtC spectra ,…”