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

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.

doi:10.1073/pnas.1815981116

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

Journal Article · 18 February 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1815981116 · OSTI ID:1506234

^[1]; Kroll, Thomas ^[2]; Baker, Michael L. ^[1]; Wilson, Samuel A. ^[1]; Decréau, Richard ^[3]; Lundberg, Marcus ^[4]; Sokaras, Dimosthenis ^[5]; Glatzel, Pieter ^[6]; Hedman, Britt ^[5]; Hodgson, Keith O. ^[2];

^[2]

Stanford Univ., Stanford, CA (United States)
Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Stanford Univ., Stanford, CA (United States); Univ. of Burgundy, Dijon (France)
Stanford Univ., Stanford, CA (United States); Uppsala Univ., Uppsala (Sweden)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
European Synchrotron Radiation Facility (ESRF), Grenoble (France)

Hemoglobin and myoglobin are oxygen-binding proteins with S = 0 heme {FeO₂}⁸active sites. The electronic structure of these sites has been the subject of much debate. This study uses Fe K-edge X-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic X-ray scattering (RIXS) to study oxyhemoglobin and a related heme {FeO₂}⁸model 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 pfpO₂and oxyhemoglobin are compared with the data for low-spin Fe^IIand Fe^III[Fe(tpp)(Im)₂]^0/+(tpp = tetra-phenyl porphyrin) compounds, which serve as heme references. The X-ray data demonstrate that pfpO₂is similar to Fe^II, while oxyhemoglobin is qualitatively similar to Fe^III, but with significant quantitative differences. Density-functional theory (DFT) calculations show that the cjontrast between pfpO₂and oxyhemoglobin is due to a distal histidine H bond to O₂and 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 pfpO₂is dominantly Fe^IIwith 6–8% Fe^IIIcharacter, while oxyhemoglobin has a very mixed wave function that has 50–77% Fe^IIIcharacter and a partially polarized Fe–O₂π-bond.

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Research Organization:: SLAC National Accelerator Lab. (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1506234

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 8 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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