X-ray absorption spectroscopic investigation of the electronic structure differences in solution and crystalline oxyhemoglobin

Hemoglobin (Hb) is the heme-containing O ₂ transport protein essential for life in all vertebrates. The resting high-spin (S = 2) ferrous form, deoxy-Hb, combines with triplet O ₂, forming diamagnetic (S = 0) oxy-Hb. Understanding this electronic structure is the key first step in understanding tran...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2013-10, Vol.110 (41), p.16333-16338
Main Authors: Wilson, Samuel A., Green, Evan, Mathews, Irimpan I., Benfatto, Maurizio, Hodgson, Keith O., Hedman, Britt, Sarangi, Ritimukta
Format: Article
Language:English
Subjects:
Absorption spectroscopy
Biological Sciences
Crystallography
Crystallography, X-Ray
Crystals
Electron spectroscopy
Electronic structure
Hemoglobins
Hydrogen bonds
Ligands
Molecular Structure
Oxidation
Oxyhemoglobins - chemistry
Physical Sciences
Porphyrins
Protein Conformation
Proteins
Spectrum analysis
Vertebrates
X-Ray Absorption Spectroscopy - methods
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Summary:Hemoglobin (Hb) is the heme-containing O ₂ transport protein essential for life in all vertebrates. The resting high-spin (S = 2) ferrous form, deoxy-Hb, combines with triplet O ₂, forming diamagnetic (S = 0) oxy-Hb. Understanding this electronic structure is the key first step in understanding transition metal–O ₂ interaction. However, despite intense spectroscopic and theoretical studies, the electronic structure description of oxy-Hb remains elusive, with at least three different descriptions proposed by Pauling, Weiss, and McClure-Goddard, based on theory, spectroscopy, and crystallography. Here, a combination of X-ray absorption spectroscopy and extended X-ray absorption fine structure, supported by density functional theory calculations, help resolve this debate. X-ray absorption spectroscopy data on solution and crystalline oxy-Hb indicate both geometric and electronic structure differences suggesting that two of the previous descriptions are correct for the Fe–O ₂ center in oxy-Hb. These results support the multiconfigurational nature of the ground state developed by theoretical results. Additionally, it is shown here that small differences in hydrogen bonding and solvation effects can tune the ground state, tipping it into one of the two probable configurations. These data underscore the importance of solution spectroscopy and show that the electronic structure in the crystalline form may not always reflect the true ground-state description in solution.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1315734110