Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex

James Yan; Thomas Kroll; Michael Baker; Samuel Wilson; Richard  Decreau; Marcus Lundberg; Dimosthenis Sokaras; Pieter Glatzel; Britt Hedman; Keith Hodgson; Edward I. Solomon

doi:10.1073/pnas.1815981116

Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex

James Yan, Thomas Kroll, Michael Baker, Samuel Wilson, Richard Decreau, Marcus Lundberg, Dimosthenis Sokaras, Pieter Glatzel, Britt Hedman, Keith Hodgson, Edward I. Solomon

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Abstract

Hemoglobin and myoglobin are oxygen-binding proteins with S =
0 heme fFeO2g8 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 Xray
scattering (RIXS) to study oxyhemoglobin and a related heme
fFeO2g8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = mesotetra(
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. 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 wavefunction that has 50-77% FeIII character and a partially
polarized Fe-O2 π bond.

Original language	English
Pages (from-to)	2854-2859
Number of pages	6
Journal	Proceedings of the National Academy of Sciences
Volume	116
Issue number	8
Early online date	4 Feb 2019
DOIs	https://doi.org/10.1073/pnas.1815981116
Publication status	Published - 4 Feb 2019

Keywords

x-ray spectroscopy
resonant inelastic x-ray scattering
DFT
oxyhemoglobin
electronic structure

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10.1073/pnas.1815981116

accepted_manuscript_PNAS_formatedAccepted author manuscript, 1.93 MB

UoMaH: The University of Manchester at Harwell
Lawrence, J. (PI), Burnett, T. (PI), Baker, M. (Researcher), Eastwood, D. (Researcher), Falkowska, M. (Researcher), Freitas, D. (Researcher), Hunt, S. (Researcher), Khan, A. (Researcher), Lane, H. (Researcher), Lezcano Gonzalez, I. (Researcher), Ma, L. (Researcher), Mirihanage, W. (Researcher), Parlett, C. (Researcher), Xu, S. (Researcher), Yan, K. (Researcher), Reinhard, C. (Support team), Duggins, D. (Technical team), Lewis-Fell, J. (Technical team), Nonni, S. (Technical team), Rollings, B. (Technical team), Sinclair, L. (Technical team) & Batts, S. (Support team)
1/01/18 → …
Project: Other

Cite this

Yan, J., Kroll, T., Baker, M., Wilson, S., Decreau, R., Lundberg, M., Sokaras, D., Glatzel, P., Hedman, B., Hodgson, K., & Solomon, E. I. (2019). Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex. Proceedings of the National Academy of Sciences, 116(8), 2854-2859. https://doi.org/10.1073/pnas.1815981116

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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 fFeO2g8 active sites. The electronic structure of these siteshas been the subject of much debate. This study utilizes Fe K-edgeX-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic Xrayscattering (RIXS) to study oxyhemoglobin and a related hemefFeO2g8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = mesotetra(α,α,α,α-o-pivalamido-phenyl)porphyrin, or TpivPP, 1-MeIm =1-methylimidazole) (pfpO2), which was previously analyzed usingL-edge XAS. The K-edge XAS and RIXS data of pfpO2 and oxyhemoglobinare compared with the data for low-spin FeII andFeIII [Fe(tpp)(Im)2]0/+ (tpp = tetra-phenyl porphyrin) compounds,which serve as heme references. The X-ray data show that pfpO2is similar to FeII, while oxyhemoglobin is qualitatively similar toFeIII, but with significant quantitative differences. DFT calculationsshow that the difference between pfpO2 and oxyhemoglobin isdue to a distal histidine H-bond to O2 and the less hydrophobicenvironment in the protein, which lead to more backbonding intothe O2. A valence bond configuration interaction multiplet modelis used to analyze the RIXS data and show that pfpO2 is dominantlyFeII with 6-8% FeIII character, while oxyhemoglobin has a verymixed wavefunction that has 50-77% FeIII character and a partiallypolarized Fe-O2 π bond.",

keywords = "x-ray spectroscopy, resonant inelastic x-ray scattering, DFT, oxyhemoglobin, electronic structure",

author = "James Yan and Thomas Kroll and Michael Baker and Samuel Wilson and Richard Decreau and Marcus Lundberg and Dimosthenis Sokaras and Pieter Glatzel and Britt Hedman and Keith Hodgson and Solomon, {Edward I.}",

year = "2019",

month = feb,

day = "4",

doi = "10.1073/pnas.1815981116",

language = "English",

volume = "116",

pages = "2854--2859",

journal = "Proceedings of the National Academy of Sciences",

issn = "0027-8424",

publisher = "National Academy of Sciences",

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Yan, J, Kroll, T, Baker, M, Wilson, S, Decreau, R, Lundberg, M, Sokaras, D, Glatzel, P, Hedman, B, Hodgson, K & Solomon, EI 2019, 'Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex', Proceedings of the National Academy of Sciences, vol. 116, no. 8, pp. 2854-2859. https://doi.org/10.1073/pnas.1815981116

TY - JOUR

T1 - Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex

AU - Yan, James

AU - Kroll, Thomas

AU - Baker, Michael

AU - Wilson, Samuel

AU - Decreau, Richard

AU - Lundberg, Marcus

AU - Sokaras, Dimosthenis

AU - Glatzel, Pieter

AU - Hedman, Britt

AU - Hodgson, Keith

AU - Solomon, Edward I.

PY - 2019/2/4

Y1 - 2019/2/4

N2 - Hemoglobin and myoglobin are oxygen-binding proteins with S =0 heme fFeO2g8 active sites. The electronic structure of these siteshas been the subject of much debate. This study utilizes Fe K-edgeX-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic Xrayscattering (RIXS) to study oxyhemoglobin and a related hemefFeO2g8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = mesotetra(α,α,α,α-o-pivalamido-phenyl)porphyrin, or TpivPP, 1-MeIm =1-methylimidazole) (pfpO2), which was previously analyzed usingL-edge XAS. The K-edge XAS and RIXS data of pfpO2 and oxyhemoglobinare compared with the data for low-spin FeII andFeIII [Fe(tpp)(Im)2]0/+ (tpp = tetra-phenyl porphyrin) compounds,which serve as heme references. The X-ray data show that pfpO2is similar to FeII, while oxyhemoglobin is qualitatively similar toFeIII, but with significant quantitative differences. DFT calculationsshow that the difference between pfpO2 and oxyhemoglobin isdue to a distal histidine H-bond to O2 and the less hydrophobicenvironment in the protein, which lead to more backbonding intothe O2. A valence bond configuration interaction multiplet modelis used to analyze the RIXS data and show that pfpO2 is dominantlyFeII with 6-8% FeIII character, while oxyhemoglobin has a verymixed wavefunction that has 50-77% FeIII character and a partiallypolarized Fe-O2 π bond.

AB - Hemoglobin and myoglobin are oxygen-binding proteins with S =0 heme fFeO2g8 active sites. The electronic structure of these siteshas been the subject of much debate. This study utilizes Fe K-edgeX-ray absorption spectroscopy (XAS) and 1s2p resonant inelastic Xrayscattering (RIXS) to study oxyhemoglobin and a related hemefFeO2g8 model compound, [(pfp)Fe(1-MeIm)(O2)] (pfp = mesotetra(α,α,α,α-o-pivalamido-phenyl)porphyrin, or TpivPP, 1-MeIm =1-methylimidazole) (pfpO2), which was previously analyzed usingL-edge XAS. The K-edge XAS and RIXS data of pfpO2 and oxyhemoglobinare compared with the data for low-spin FeII andFeIII [Fe(tpp)(Im)2]0/+ (tpp = tetra-phenyl porphyrin) compounds,which serve as heme references. The X-ray data show that pfpO2is similar to FeII, while oxyhemoglobin is qualitatively similar toFeIII, but with significant quantitative differences. DFT calculationsshow that the difference between pfpO2 and oxyhemoglobin isdue to a distal histidine H-bond to O2 and the less hydrophobicenvironment in the protein, which lead to more backbonding intothe O2. A valence bond configuration interaction multiplet modelis used to analyze the RIXS data and show that pfpO2 is dominantlyFeII with 6-8% FeIII character, while oxyhemoglobin has a verymixed wavefunction that has 50-77% FeIII character and a partiallypolarized Fe-O2 π bond.

KW - x-ray spectroscopy

KW - resonant inelastic x-ray scattering

KW - DFT

KW - oxyhemoglobin

KW - electronic structure

U2 - 10.1073/pnas.1815981116

DO - 10.1073/pnas.1815981116

M3 - Article

C2 - 30718404

SN - 0027-8424

VL - 116

SP - 2854

EP - 2859

JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

IS - 8

ER -

Resonant Inelastic X-Ray Scattering Determination of the Electronic Structure of Oxyhemoglobin and Its Model Complex

Abstract

Keywords

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UoMaH: The University of Manchester at Harwell

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