Unique Structural and Electronic Features of Perferryl–Oxo Oxidant in Cytochrome P450

We have performed hybrid density functional theory (DFT) calculations on the geometric and electronic structures of low-lying doublet and quartet ferryl–oxo [Fe(IV)O] oxidants and a doublet perferryl–oxo [Fe(V)O] oxidant in Cytochrome P450. Fully optimized structures of compound I models have been determined, and the proper symmetry of wave functions has been restored by the spin-projection technique. The results show that the perferryl–oxo species is relatively low lying, as compared with the excited state of the ferryl–oxo species, if the iron–oxo bond is properly described as the mixing of several appropriate excited electronic configurations to minimize electron repulsion. This means that the perferryl–oxo species is virtually in a mixed-valent resonance state, ↑Fe(V)O ↔ ↑Fe(IV)•↑–↓•O, containing a highly reactive pπ atomic oxygen radical. The anionic thiolate ligand acts as a Lewis σ base and functions to achieve the stability of the perferryl–oxo complex and to activate the oxo ligand trans to it by asymmetric bond distortion along the O–Fe–S axis by lengthening the Fe–O bond and shortening the Fe–S bond, prior to the hydrogen-atom abstraction from the substrate.