Skeletal substituents and the distal environment determine the spin state of natural and synthetic iron porphyrins: role in the O2 reduction reaction

Abstract

The poprhyrin structure, along with its axial ligands and surrounding environment determine its electronic structure which results in a wide range of reduction potentials and different spin states of the iron center in heme enzymes in nature. Tuning these electronic structure attributes is crucial for heme proteins to be able to efficiently catalyze multiproton and multielectron reduction of small molecules such as O₂, NO₂⁻ and SO₂, which have very different reduction potentials, and this is important in designing small-molecule catalysts for these energy- and environment-related transformations. However, deconvoluting the effects of porphyrin modifications and protein environments on the electronic structures of active sites is often difficult. Site-isolated imidazole-bound heme b, diacetyl heme and their synthetic analogue active sites are created atop self-assembled monolayers of thiols on Au electrodes. In situ surface-enhanced resonance Raman spectroscopy indicates that imidazole-bound heme b prefers a low-spin active site in both its redox states in contrast to the protein active sites with a histidine-bound heme b cofactor, which are all high spin. The imidazole-bound diacetyl heme, with electron-withdrawing groups like that of heme a, however, prefers a high-spin ground state under the same conditions. Imidazole-bound synthetic iron porphyrins show that the ground state gradually changes from low spin, in iron tetraphenyl porphyrin, to high spin as electron-withdrawing groups are attached to the porphyrin ligand. When the solvent-exposed site of a low-spin iron porphyrin is hydrophobic, it switches to its high-spin state. The electron-withdrawing groups and the spin state can tune the reduction potential of imidazole-bound iron porphyrins by more than 300 mV. The high-spin ground state allows faster electrocatalytic O₂ reduction at a lower overpotential, while the low-spin ground state stays inhibited due to product inhibition.