Structure and spectra of ferrous dioxygen and reduced ferrous dioxygen model cytochrome P450

The optimized geometries of the stable ferrous dioxygen and transient reduced ferrous dioxygen forms of a methylmercaptate porphine model of the cytochrome P450 heme system were calculated using nonlocal density functional theoretical (DFT) methods. The optimized geometry of the ferrous dioxygen form is in good agreement with the structure of a model compound of this species and the calculated diamagnetic singlet ground state is consistent with the reported lack of ESR spectrum of this species. The calculated ground state of the reduced ferrous dioxygen species is a low-spin (doublet) state, in agreement with the reported ESR signature of this species in P450cam. The dioxygen ligand in the reduced form is shown to preferentially bind to the heme iron in an asymmetric "end-on" geometry. The most pronounced structural effects of the reduction of the ferrous dioxygen species are the elongation of the Fe-O and Fe-S bonds. This bond lengthening is due to the addition of an electron into a molecular orbital of significant antibonding character in the S-Fe-O bonding upon reduction of the ferrous dioxygen species. The molecular electrostatic potential of the ferrous dioxygen and reduced ferrous dioxygen P450 intermediates both have pronounced minima near each of the bound dioxygen atoms, but with significantly lower minima in the reduced species. INDO/S/CI calculations of spectral and electronic properties were performed at the computed density functional geometries. The diamagnetic singlet ground state of the ferrous dioxygen and the doublet ground state of the reduced ferrous dioxygen species found with inclusion of configuration interaction are in agreement with the DFT results. The INDO/S/CI spectra of the ferrous dioxygen and reduced ferrous dioxygen species both have a split Soret band, due to mixing of the sulfur p orbitals with the porphyrin pi orbitals modulated by the dioxygen ligands. Comparison of the computed spectra of these species with the reported experimental spectra show similar split-Sorer signatures and spectral shifts compared to the ferric high-spin substrate bound state, The agreement between calculated and experimental spectra provides additional evidence that the species which are the origin of the observed spectra are indeed the ferrous dioxygen and reduced ferrous dioxygen P450 species.