Electronic and Geometrical Structures of Hemes a/a3 of the Bovine Cytochrome c Oxidase in the Fully-Reduced and Oxidized States Revealed by ab Inito Calculations

Abstract

In the respiration process, cytochrome c oxidase (CcO) plays a crucial role; i.e., it generates the gradient of the proton concentration between a matrix and an intermembrane space of the mitochondria, exploiting the free energy released by the catalysis where an oxygen atom is reduced to two water molecules. For this reaction, the required electrons/protons are transferred to the heme a site and the heme a3-CuB site of CcO. Then, the catalytic reaction and proton pumping process are simultaneously occurred through these sites. In this way, the heme systems act as “hub”, which is essential to understand the functional mechanisms of CcO.In this study, to investigate the electronic structures of the heme systems, the Wannier function centers (WFCs) were employed. The WFCs correspond to the centers of maximally localized orthogonal functions termed the Wannier functions, and the concept of WFCs is similar to the Lewis view of the molecular bonds. Accordingly, this may provide convenient pictures of electronic structures based on chemical intuitions.Using the bovine CcO structures, we constructed isolated models, each of which contains a heme and a histidine ligand, and performed geometry optimizations using ab initio DFT/HF hybrid all-electron calculations at the B3LYP functional level. Then, using the wave functions calculated for each of the heme systems, we obtained Wannier functions and WFCs. As a result, we have found that the imidazole ring of the histidine ligand are rotated in both the reduced and oxidized states, and are strongly associated with the polarization of the heme systems. In CcO, the hemes contact with the amino acid residues through van der Waals interactions, which could regulate the electronic structures of the heme systems.