PNNL

Abstract

Ferric and ferrous hemes, such as those present in electron transfer proteins, often have low-lying spin states that are very close in energy. In order 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 complex consists of an iron-porphyrin axially ligated by two imidazoles, which model the attachment of the hemes to cytochrome histidines. Using the B3LYP hybrid functional, we found that, in the ferric model heme complex, the doublet is lower in energy than the sextet by 8.60 kcal/mol, and the singlet ferrous heme is 7.60 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 5.21 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 dxy orbital is most likely involved in the electron transfer between neighboring hemes (the xy-plane is the plane of the porphyrin). The B3LYP electronic structure was verified by the calculated Mossbauer parameters, which are consistent with experimental values, and isotropic hyperfine coupling constants were evaluated for the ligand nitrogen atoms in each of the hemes. 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 model hemes, which suggests that the protein environment, modeled here by the imidazoles, plays an important role in regulating the spin state.