Nonadiabatic electronic spin transition in ligand–heme protein binding kinetics and the influence of the heme Fe molecular environment

Abstract

Nonadiabatic spin transitions can significantly reduce rates in reactions involving transition metals. Zero field spin splittings can further modulate the reaction rate at temperatures with thermal energies of the same size as the zero field splittings, and the low temperature reaction rate can be completely shut off in ligand fields of relatively low symmetry, C2v or D2, for example, due to a vanishing of the electronic matrix element between the initial and final ground spin states. We show in this paper that if the site symmetry is lowered even further, the electronic matrix element coupling the ground spin states can become nonzero, allowing the reaction to occur as the temperature approaches zero. We show what factors in the metal’s ligand environment are important for the electronic coupling between the initial and final electronic states. This is especially relevant for transition metals in sites of low symmetry, such as are found in biomolecules. We focus specifically on heme proteins and show how factors in the immediate environment of the Fe, such as the proximal histidine, may lower the site symmetry sufficiently to allow a nonzero low temperature nonadiabatic electronic spin transition that may be necessary for ligand binding. We also use these ideas to make predictions that could resolve the question of whether the reversible binding of CO to heme proteins is a nonadiabatic electronic process.