Experimental and Theoretical Correlations Between Vanadium K‑Edge X‑Ray Absorption and Kβ Emission Spectra

J Biol Inorg Chem DOI 10.1007/s00775-016-1358-7 ORIGINAL PAPER Experimental and theoretical correlations between vanadium K-edge X-ray absorption and Kβ emission spectra Julian A. Rees1,2 · Aleksandra Wandzilak1,3 · Dimitrios Maganas1 · Nicole I. C. Wurster1 · Stefan Hugenbruch1 · Joanna K. Kowalska1 · Christopher J. Pollock1,7 · Frederico A. Lima5 · Kenneth D. Finkelstein6 · Serena DeBeer1,4 Received: 22 March 2016 / Accepted: 29 April 2016 © The Author(s) 2016. This article is published with open access at Springerlink.com Abstract A series of vanadium compounds was studied establish correction factors for the computational protocols by K-edge X-ray absorption (XAS) and Kβ X-ray emis- through calibration to experiment. These hard X-ray meth- sion spectroscopies (XES). Qualitative trends within the ods can probe vanadium ions in any oxidation or spin state, datasets, as well as comparisons between the XAS and XES and can readily be applied to sample environments ranging data, illustrate the information content of both methods. The from solid-phase catalysts to biological samples in frozen complementary nature of the chemical insight highlights solution. Thus, the combined XAS and XES approach, cou- the success of this dual-technique approach in character- pled with DFT calculations, provides a robust tool for the izing both the structural and electronic properties of vana- study of vanadium atoms in bioinorganic chemistry. dium sites. In particular, and in contrast to XAS or extended X-ray absorption fine structure (EXAFS), we demonstrate Keywords Vanadium · X-ray spectroscopy · Density that valence-to-core XES is capable of differentiating functional theory DFT · XES · XAS between ligating atoms with the same identity but different bonding character. Finally, density functional theory (DFT) and time-dependent DFT calculations enable a more Introduction detailed, quantitative interpretation of the data. We also Vanadium plays an essential role in both biochemical and industrial catalysis. A number of solid-state cata- In honor of Professor Edward I. Solomon’s 2016 ACS Alfred lysts employ vanadium in various oxide-type formula- Bader Award. tions, notably for the oxidative dehydrogenation of short J. A. Rees and A. Wandzilak contributed equally to this work. chain alkanes; a highly desirable chemical transformation [1, 2]. While the natural abundance of vanadium is only Electronic supplementary material The online version of this 0.015 % in the earth’s crust, it is found in the oceans at article (doi:10.1007/s00775-016-1358-7) contains supplementary material, which is available to authorized users. * Serena DeBeer 5 Centro Nacional de Pesquisa em Energia e Materiais, [email protected] Laboratório Nacional de Luz Síncrotron, Rua Giuseppe Máximo Scolfaro 10000, Campinas, SP 13083‑970, Brazil 1 Max Planck Institute for Chemical Energy Conversion, 6 Cornell High Energy Synchrotron Source, Wilson Stiftstr. 34‑36, 45470 Mülheim an der Ruhr, Germany Laboratory, Cornell University, Ithaca, NY 14853, USA 2 Department of Chemistry, University of Washington, 7 Department of Chemistry, The Pennsylvania State University, Box 351700, Seattle, WA 98195‑1700, USA University Park, PA 16802, USA 3 Faculty of Physics and Applied Computer Science, AGH University of Science and Technology, al. Mickiewicza 30, 30‑059 Kraków, Poland 4 Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853, USA 1 3 J Biol Inorg Chem concentrations as high as 30 nM, making it readily bioa- resonance methods have specific spin-state requirements, vailable [3]. At physiological conditions, vanadium is sta- certain intermediates may be spectroscopically “silent”, ble in the 3 to 5 oxidation states, and in its most oxi- rendering NMR and EPR unsuitable to probe certain steps + + dized forms is a potent Lewis acid. It is most commonly during a catalytic cycle. Thus, the advancement of addi- 3− found in biology as some form of the vanadate ion, VO4 , tional biologically amenable spectroscopic techniques, par- though some enzymes that promote mostly oxidative trans- ticularly those capable of probing a variety of changes in formations require vanadium as a metallocofactor [4–6]. electronic structure without preference for oxidation or spin For example, vanadium-dependent haloperoxidases pro- state, is highly desirable. Herein, we describe a combined mote the two-electron oxidation of halides using hydrogen X-ray spectroscopic study, utilizing both V K-edge XAS peroxide as the terminal oxidant, or, in the absence of an and Kβ X-ray emission spectroscopies (XES). Calibration organic substrate, can perform halide-dependent catalase- to density functional theory (DFT) calculations provides an like disproportionation of hydrogen peroxide to water and insightful, element-specific probe of vanadium geometric dioxygen [7]. These haloperoxidases can also catalyze and electronic structure, using experimental methods well the oxidation of thioethers to sulfoxides, exhibiting oxo- adapted to the study of biological molecules. transfer reactivity that is well established for high-valent In K-edge XAS, a 1s electron is excited into either bound vanadium complexes [8]. Interestingly, this sulfoxidation states or to the continuum. In the former case, transitions chemistry is the inverse of the reaction catalyzed by some into singly or unoccupied 3d orbitals of a first-row transition molybdenum-dependent oxotransferases, such as DMSO metal give rise to the pre-edge region, which can provide reductase, which generate thioethers from the correspond- insight into the energies of the 3d manifold. Additionally, the ing sulfoxide substrate at a molybdopterin active site [3]. intensities of these 1s → 3d transitions, while formally quad- The diagonal relation of molybdenum and vanadium rupolar, are largely governed by metal p–d mixing, and thus and their use in similar, albeit complementary, biochemi- the dipole selection rule [26, 27]. Changes in metal–ligand cal sulfoxidation reactivity serves to further highlight their bond covalency [28] and geometric distortion from cen- involvement in the promotion of arguably nature’s most trosymmetry both serve to modulate the intensity of the pre- complex chemical transformation: the six-electron reduc- edge transitions through perturbations in p–d mixing [29]. tion of aerial dinitrogen. Biological nitrogen fixation is Time-dependent DFT (TD-DFT) calculations have proven catalyzed by the nitrogenase enzymes, which contain three capable of correctly predicting relative energies and intensi- distinct types of [Fe–S] clusters. A [4Fe–4S] cluster in the ties of these pre-edge features, and through careful analysis Fe protein provides reducing equivalents via hydrolysis of and comparison to experiment, additional insight into geo- ATP, while in the MoFe or VFe protein an [8Fe–7S] P-clus- metric and electronic structure can be obtained [26, 30, 31]. ter serves as an electron transfer relay, reducing the active Even with the aid of theoretical insight, however, probing the site [M–7Fe–9S–C] cofactor, where M Mo or V [9–14]. electronic structure of ligand-based orbitals is a challenge = Extensive studies of these enzymes using a range of spec- for XAS, and in this area, XES holds significant promise. troscopic techniques continue to provide novel insight into Following the 1s ionization described above, in a one- the structure and function of nitrogenase; however, signif- electron picture, Kβ emission is the fluorescent decay of icant questions such as the role of the heterometal or the an electron from the n = 3 shell into a 1s core hole. In the location of N2 binding still remain unanswered [12, 15–19]. case of first-row transition metals, for which these are the In many of these enzymes, the identities of important valence levels, the different regions in the Kβ spectrum intermediates, often including the catalytically compe- provide complementary chemical insight. The Kβ mainline tent species, are still unknown. Characterization of the feature arises from metal 3p → 1s transitions, and is sen- spin state, oxidation state, and coordination environment sitive to the oxidation state and local spin at the absorber of vanadium in a catalytic cycle are important prerequi- atom [32–34]. This dipole-allowed transition is intense, and sites for mechanistic understanding. Existing methods is readily observable in low concentrations of metal atom often utilized in such studies include 51V nuclear mag- emitter. The K-beta mainline has seen extensive prior use netic resonance (NMR) [20] and various pulsed electron as a marker for oxidation and spin state, as the number of paramagnetic resonance (EPR) spectroscopies, [21, 22] as unpaired 3d electrons modulates the 3p–3d exchange cou- well as X-ray-based methods: vanadium K- and L-edge pling, and thus the multiplet-derived energetic splitting of X-ray absorption spectroscopy (XAS) and extended X-ray the Kβ mainline peaks. However, care must be taken in the absorption fine structure (EXAFS) [23–25]. Some of these interpretation of this splitting, as we have recently shown techniques have limited applicability to enzyme systems, that the spectral features can be significantly modulated by however. For example, L-edge XAS experiments are con- metal–ligand covalency [34–37]. ducted in high-vacuum environments not ordinarily ame- To higher energy, the weaker valence-to-core (VtC) nable to biological samples. Furthermore, as magnetic region of the Kβ XES spectrum probes the valence shell,

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