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Title: 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}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 FeIIand FeIII[Fe(tpp)(Im)2]0/+(tpp = tetra-phenyl porphyrin) compounds, which serve as heme references. The X-ray data demonstrate that pfpO2is similar to FeII, while oxyhemoglobin is qualitatively similar to FeIII, 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 FeIIwith 6–8% FeIIIcharacter, while oxyhemoglobin has a very mixed wave function that has 50–77% FeIIIcharacter and a partially polarized Fe–O2π-bond.

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [3];  [4];  [5];  [6];  [5];  [2]; ORCiD logo [2]
  1. Stanford Univ., Stanford, CA (United States)
  2. Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
  3. Stanford Univ., Stanford, CA (United States); Univ. of Burgundy, Dijon (France)
  4. Stanford Univ., Stanford, CA (United States); Uppsala Univ., Uppsala (Sweden)
  5. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  6. European Synchrotron Radiation Facility (ESRF), Grenoble (France)
Publication Date:
Research Org.:
SLAC National Accelerator Lab. (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1506234
Grant/Contract Number:  
AC02-76SF00515; GM-40392; P41GM103393; KR3611/2-1
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 8; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; X-ray spectroscopy; resonant inelastic X-ray; scattering; DFT; oxyhemoglobin; electronic structure

Citation Formats

Yan, James J., Kroll, Thomas, Baker, Michael L., Wilson, Samuel A., Decréau, Richard, Lundberg, Marcus, Sokaras, Dimosthenis, Glatzel, Pieter, Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex. United States: N. p., 2019. Web. doi:10.1073/pnas.1815981116.
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. Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex. United States. doi:10.1073/pnas.1815981116.
Yan, James J., Kroll, Thomas, Baker, Michael L., Wilson, Samuel A., Decréau, Richard, Lundberg, Marcus, Sokaras, Dimosthenis, Glatzel, Pieter, Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. Tue . "Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex". United States. doi:10.1073/pnas.1815981116. https://www.osti.gov/servlets/purl/1506234.
@article{osti_1506234,
title = {Resonant inelastic X-ray scattering determination of the electronic structure of oxyhemoglobin and its model complex},
author = {Yan, James J. and Kroll, Thomas and Baker, Michael L. and Wilson, Samuel A. and Decréau, Richard and Lundberg, Marcus and Sokaras, Dimosthenis and Glatzel, Pieter and Hedman, Britt and Hodgson, Keith O. and Solomon, Edward I.},
abstractNote = {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 FeIIand FeIII[Fe(tpp)(Im)2]0/+(tpp = tetra-phenyl porphyrin) compounds, which serve as heme references. The X-ray data demonstrate that pfpO2is similar to FeII, while oxyhemoglobin is qualitatively similar to FeIII, 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 FeIIwith 6–8% FeIIIcharacter, while oxyhemoglobin has a very mixed wave function that has 50–77% FeIIIcharacter and a partially polarized Fe–O2π-bond.},
doi = {10.1073/pnas.1815981116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 8,
volume = 116,
place = {United States},
year = {2019},
month = {2}
}

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