Abstract
We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O(2) to a realistic model of ferrous deoxyheme. Beyond a Fe-O distance of approximately 2.5 A, we find a broad crossing region with five electronic states within 15 kJ/mol. The almost parallel surfaces strongly facilitate spin inversion, which is necessary in the reaction of O(2) with heme (deoxyheme is a quintet and O(2) a triplet, whereas oxyheme is a singlet). Thus, despite a small spin-orbit coupling in heme, the transition probability approaches unity. Using reasonable parameters, we estimate a transition probability of 0.06-1, which is at least 15 times larger than for the nonbiological Fe-O(+) system. Spin crossing is anticipated between the singlet ground state of bound oxyheme, the triplet and septet dissociation states, and a quintet intermediate state. The fact that the quintet state is close in energy to the dissociation couple is of biological importance, because it explains how both spin states of O(2) may bind to heme, thereby increasing the overall efficiency of oxygen binding. The activation barrier is estimated to be <15 kJ/mol based on our results and Mössbauer experiments. Our results indicate that both the activation energy and the spin-transition probability are tuned by the porphyrin as well as by the choice of the proximal heme ligand, which is a histidine in the globins. Together, they may accelerate O(2) binding to iron by approximately 10(11) compared with the Fe-O(+) system. A similar near degeneracy between spin states is observed in a ferric deoxyheme model with the histidine ligand hydrogen bonded to a carboxylate group, i.e. a model of heme peroxidases, which bind H(2)O(2) in this oxidation state.
Highlights
We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O2 to a realistic model of ferrous deoxyheme
Our results indicate that both the activation energy and the spin-transition probability are tuned by the porphyrin as well as by the choice of the proximal heme ligand, which is a histidine in the globins
We show that porphyrin is an ideal iron ligand for the spin transition problem, because it tunes the spin states to be close in energy, giving parallel binding curves, small activation energies, and large transition probabilities
Summary
We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O2 to a realistic model of ferrous deoxyheme. Reactions between singlet and triplet states are formally spin-forbidden, which means that they are slow This is the reason why organic matter may exist in an atmosphere containing much O2. Transition metals often have several excited states with unpaired electrons close in energy to the ground state This can be used to enhance the probability of spin inversion. One of the most simple biological reactions involving molecular oxygen is the binding of O2 to hemoglobin, i.e. the binding of O2 to the Fe(II) ion in a heme group This reaction is formally spin-forbidden, because the reactant deoxyheme contains four unpaired electrons in the 3d orbitals of iron (it is a quintet), and triplet O2 has two unpaired electrons. The movement of iron into the heme plane is assumed to trigger a transition from a tense state to a relaxed state after the binding of two oxygen molecules, and this trigger, in the form of the Fe–Nax pull, depends on the spin state of heme
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