Electronic Structure of Six-Coordinate Iron(III)−Porphyrin NO Adducts: The Elusive Iron(III)−NO(radical) State and Its Influence on the Properties of These Complexes

Abstract

This paper investigates the interaction between five-coordinate ferric hemes with bound axial imidazole ligands and nitric oxide (NO). The corresponding model complex, [Fe(TPP)(MI)(NO)](BF4) (MI = 1-methylimidazole), is studied using vibrational spectroscopy coupled to normal coordinate analysis and density functional theory (DFT) calculations. In particular, nuclear resonance vibrational spectroscopy is used to identify the Fe−N(O) stretching vibration. The results reveal the usual Fe(II)−NO+ ground state for this complex, which is characterized by strong Fe−NO and N−O bonds, with Fe−NO and N−O force constants of 3.92 and 15.18 mdyn/Å, respectively. This is related to two strong π back-bonds between Fe(II) and NO+. The alternative ground state, low-spin Fe(III)−NO(radical) (S = 0), is then investigated. DFT calculations show that this state exists as a stable minimum at a surprisingly low energy of only ∼1−3 kcal/mol above the Fe(II)−NO+ ground state. In addition, the Fe(II)−NO+ potential energy surface (PES) crosses the low-spin Fe(III)−NO(radical) energy surface at a very small elongation (only 0.05−0.1 Å) of the Fe−NO bond from the equilibrium distance. This implies that ferric heme nitrosyls with the latter ground state might exist, particularly with axial thiolate (cysteinate) coordination as observed in P450-type enzymes. Importantly, the low-spin Fe(III)−NO(radical) state has very different properties than the Fe(II)−NO+ state. Specifically, the Fe−NO and N−O bonds are distinctively weaker, showing Fe−NO and N−O force constants of only 2.26 and 13.72 mdyn/Å, respectively. The PES calculations further reveal that the thermodynamic weakness of the Fe−NO bond in ferric heme nitrosyls is an intrinsic feature that relates to the properties of the high-spin Fe(III)−NO(radical) (S = 2) state that appears at low energy and is dissociative with respect to the Fe−NO bond. Altogether, release of NO from a six-coordinate ferric heme nitrosyl requires the system to pass through at least three different electronic states, a process that is remarkably complex and also unprecedented for transition-metal nitrosyls. These findings have implications not only for heme nitrosyls but also for group-8 transition-metal(III) nitrosyls in general.