Coulomb Soup of Bioenergetics: Electron Transfer in a Bacterial bc1 Complex

We report atomistic molecular dynamics simulations (200 ns) of the first, rate-limiting electron transfer in the electron transport chain in a bacterial bc(1) complex. The dynamics of the energy gap between the donor and acceptor states include slow components, on the time-scale of tens of nanoseconds. These slow time-scales are related to large-scale elastic motions of the membrane-bound protein complex, which modulate both electrostatic and induction interactions of the electron with the protein-water-lipid thermal bath. The combined effect of these interactions is a high, similar to 5 eV, reorganization energy of electron transfer as calculated from their variance. The reorganization energy does not reach equilibrium on the length of simulations and the system is nonergodic on this time-scale. To account for nonergodicity, two reorganization energies are required to describe the activation barrier, and their ratio is tuned by the relative time-scales of nuclear reorganization and of the reaction.