Spin state preference and bond formation/cleavage barriers in ferrous-dioxygen heme adducts: remarkable dependence on methodology

Abstract

The electronic structure of oxy- and aqua-bound active sites of hemoglobin (Hb) and cytochrome P450 mono oxygenase (CYP450) are investigated by applying a wide range of DFT functionals including the pure BP86, the hybrid B3LYP and the recently developed hybrid meta-GGA (M06 family). Mixed descriptions of the electronic structure and widely differing order of spin-multiplet energies are obtained depending on the functional employed. A reproduction of the experimental singlet ground state of oxy Hb was achieved by all functionals: convergence to the unrestricted broken symmetry solution was favored, except for BP86 where a direct Kohn–Sham determinant wave function was found to have the lowest energy. Ferrous-dioxygen bond cleavage for both models clearly shows preference for charge separation with superoxide liberation in the case of CYP450 (thiolate axial ligand), in comparison to liberation of a clear oxygen molecule in case of Hb. Nitric oxide bound superoxide reductase (SOR) is also investigated, as a model with a known S = 3/2 spin state; results provided by B3LYP, M06 and M06L are shown to correlate well with experimental data whereas the performance of the MP2 method was relatively poor. Fe–N bond cleavage was shown to give insight into the mechanism of hydrogen peroxide liberation in SOR.