Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex

Abstract

Hemoglobin and myoglobin are oxygen-binding proteins with S = 0 heme {FeO2}8 active sites. The electronic structure of these sites has been the subject of much debate. This study utilizes Fe K-edge X-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic X-ray scattering (RIXS) to study oxyhemoglobin and a related heme {FeO2}8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = meso-tetra(α,α,α,α-o-pivalamido-phenyl)porphyrin, or TpivPP, 1-MeIm = 1-methylimidazole) (pfpO2), which was previously analyzed using L-edge XAS. The K-edge XAS and RIXS data of pfpO2 and oxyhemoglobin are compared with the data for low-spin FeII and FeIII [Fe(tpp)(Im)2]0/+ (tpp = tetra-phenyl porphyrin) compounds, which serve as heme references. The X-ray data show that pfpO2 is similar to FeII, while oxyhemoglobin is qualitatively similar to FeIII, but with significant quantitative differences. Density-functional theory (DFT) calculations show that the difference between pfpO2 and oxyhemoglobin is due to a distal histidine H bond to O2 and the less hydrophobic environment in the protein, which lead to more backbonding into the O2. A valence bond configuration interaction multiplet model is used to analyze the RIXS data and show that pfpO2 is dominantly FeII with 6–8% FeIII character, while oxyhemoglobin has a very mixed wave function that has 50–77% FeIII character and a partially polarized Fe–O2 π-bond.

Multireference Description of Nickel–Aryl Homolytic Bond Dissociation Processes in Photoredox Catalysis

“…This highly covalent bonding framework is not particularly amenable to formal redox state assignment and is more consistent with a multireference bonding description. 45,46 PESs for Ni(II)-C bond dissociations from 1 and 2 are given in Figures 2A and S2G, respectively. The DFT BDEs are ~43 kcal mol -1 and ~31 kcal mol -1 starting from the relaxed, lowest energy singlet and triplet structures of 1, respectively, consistent with the ~32 kcal mol -1 from a study invoking thermal homolysis on the triplet PES.…”

X-ray absorption spectroscopy of exemplary platinum porphyrin and corrole derivatives: metal- versus ligand-centered oxidation

“…(Given their broad importance, there have been surprisingly few XAS and related measurements on porphyrin and corrole derivatives. [20][21][22][23][24][25][26][27][28][29][30] The results, interpreted with density functional theory (DFT) calculations, provide detailed insights into the factors inuencing the pre-edge shis of Pt complexes.…”

Synthetic heme dioxygen adducts: electronic structure and reactivity

“…•-GS for Hb-O 2 [39]. Alternatively, this H-bonding was absent in the model system, which resulted in a Fe II -O 2 -like GS electronic structure.…”

“…(Figure 1, middle) [38]. Recent developments in elucidating GS wave function using resonance inelastic X-ray scattering (RIXS) data suggest that the GS electronic configuration of Hb-O 2 / Mb-O 2 is more like Fe III -O 2 -(Figure 1, left), while dioxygen adducts of synthetic porphyrin such as Fe-picket fence possess Fe II -O 2 GS (Figure 1, middle) [39].…”