Activationless electron transfer through the hydrophobic core of cytochrome c oxidase
Abstract
Electron transfer (ET) within proteins occurs by means of chains of redox intermediates that favor directional and efficient electron delivery to an acceptor. Individual ET steps are energetically characterized by the electronic coupling V, driving force ΔG, and reorganization energy λ. λ reflects the nuclear rearrangement of the redox partners and their environment associated with the reactions; λ ≈ 700-1,100 meV (1 eV = 1.602 × 10-19 J) has been considered as a typical value for intraprotein ET. In nonphotosynthetic systems, functional ET is difficult to assess directly. However, using femtosecond flash photolysis of the CO-poised membrane protein cytochrome c oxidase, the intrinsic rate constant of the low-ΔG electron injection from heme a into the heme a 3-CuB active site was recently established at (1.4 ns)-1. Here, we determine the temperature dependence of both the rate constant and ΔG of this reaction and establish that this reaction is activationless. Using a quantum mechanical form of nonadiabatic ET theory and common assumptions for the coupled vibrational modes, we deduce that λ is <200 meV. It is demonstrated that the previously accepted value of 760 meV actually originates from the temperature dependence of CuB-CO bond breaking. We discuss that low-ΔG, low-λ reactions are common for efficiently channeling electrons through chains that are buried inside membrane proteins.