TY - JOUR
T1 - Characterization of electronic structure and properties of a bis(histidine) heme model complex
AU - Smith, Dayle M.A.
AU - Dupuis, Michel
AU - Vorpagel, Erich R.
AU - Straatsma, T. P.
PY - 2003/3/5
Y1 - 2003/3/5
N2 - Ferric and ferrous hemes, such as those present in electron transfer proteins, often have low-lying spin states that are very close in energy. To explore the relationship between spin state, geometry, and cytochrome electron transfer, we investigate, using density functional theory, the relative energies, electronic structure, and optimized geometries for a high- and low-spin ferric and ferrous heme model complex. Our model consists of an iron-porphyrin axially ligated by two imidazoles, which model the interaction of a heme with histidine residues. Using the B3LYP hybrid functional, we found that, in the ferric model heme complex, the doublet is lower in energy than the sextet by 8.4 kcal/mol and the singlet ferrous heme is 6.7 kcal/mol more stable than the quintet. The difference between the high-spin ferric and ferrous model heme energies yields an adiabatic electron affinity (AEA) of 5.24 eV, and the low-spin AEA is 5.17 eV. Both values are large enough to ensure electron trapping, and electronic structure analysis indicates that the iron dπ orbital is involved in the electron transfer between hemes. Mössbauer parameters calculated to verify the B3LYP electronic structure correlate very well with experimental values. Isotropic hyperfine coupling constants for the ligand nitrogen atoms were also evaluated. The optimized geometries of the ferric and ferrous hemes are consistent with structures from X-ray crystallography and reveal that the iron-imidazole distances are significantly longer in the high-spin hemes, which suggests that the protein environment, modeled here by the imidazoles, plays an important role in regulating the spin state. Iron-imidazole dissociation energies, force constants, and harmonic frequencies were calculated for the ferric and ferrous low-spin and high-spin hemes. In both the ferric and the ferrous cases, a single imidazole ligand is more easily dissociated from the high-spin hemes.
AB - Ferric and ferrous hemes, such as those present in electron transfer proteins, often have low-lying spin states that are very close in energy. To explore the relationship between spin state, geometry, and cytochrome electron transfer, we investigate, using density functional theory, the relative energies, electronic structure, and optimized geometries for a high- and low-spin ferric and ferrous heme model complex. Our model consists of an iron-porphyrin axially ligated by two imidazoles, which model the interaction of a heme with histidine residues. Using the B3LYP hybrid functional, we found that, in the ferric model heme complex, the doublet is lower in energy than the sextet by 8.4 kcal/mol and the singlet ferrous heme is 6.7 kcal/mol more stable than the quintet. The difference between the high-spin ferric and ferrous model heme energies yields an adiabatic electron affinity (AEA) of 5.24 eV, and the low-spin AEA is 5.17 eV. Both values are large enough to ensure electron trapping, and electronic structure analysis indicates that the iron dπ orbital is involved in the electron transfer between hemes. Mössbauer parameters calculated to verify the B3LYP electronic structure correlate very well with experimental values. Isotropic hyperfine coupling constants for the ligand nitrogen atoms were also evaluated. The optimized geometries of the ferric and ferrous hemes are consistent with structures from X-ray crystallography and reveal that the iron-imidazole distances are significantly longer in the high-spin hemes, which suggests that the protein environment, modeled here by the imidazoles, plays an important role in regulating the spin state. Iron-imidazole dissociation energies, force constants, and harmonic frequencies were calculated for the ferric and ferrous low-spin and high-spin hemes. In both the ferric and the ferrous cases, a single imidazole ligand is more easily dissociated from the high-spin hemes.
UR - http://www.scopus.com/inward/record.url?scp=0037420328&partnerID=8YFLogxK
U2 - 10.1021/ja0280473
DO - 10.1021/ja0280473
M3 - Article
C2 - 12603159
AN - SCOPUS:0037420328
SN - 0002-7863
VL - 125
SP - 2711
EP - 2717
JO - Journal of the American Chemical Society
JF - Journal of the American Chemical Society
IS - 9
ER -