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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 8; pp. 2854 - 2859
• Main Authors: Yan, James J., Kroll, Thomas, Baker, Michael L., Wilson, Samuel A., Decréau, Richard, Lundberg, Marcus, Sokaras, Dimosthenis, Glatzel, Pieter, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 19.02.2019; National Academy of Sciences, Washington, DC (United States)
• Subjects: Absorption spectroscopy; Catalytic Domain; Configuration interaction; Data processing; Density functional theory; DFT; Electronic structure; Ferric Compounds - chemistry; Heme; Heme - chemistry; Hemoglobin; Histidine; Hydrogen bonds; Hydrophobicity; Inelastic scattering; INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Iron - chemistry; Metalloporphyrins - chemistry; Models, Molecular; Myoglobin - chemistry; Myoglobins; Oxygen - chemistry; Oxyhemoglobin; Oxyhemoglobins - chemistry; Physical Sciences; Porphyrins - chemistry; Proteins; resonant inelastic X-ray; resonant inelastic X-ray scattering; scattering; Scattering, Radiation; X ray absorption; X-Ray Absorption Spectroscopy; X-ray scattering; X-ray spectroscopy; X-Rays; resonant inelastic X-ray scattering; DFT; X-ray spectroscopy; oxyhemoglobin; electronic structure
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1815981116

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 back-bonding 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.