A molecular breakwater enhances electron transfer between proteins

Does natural selection optimize molecular biomachinery at the quantum level? We present statistical characterizations of molecular dynamics at an interprotein electron transfer (ET) interface. In simulations of the wild-type protein complex, we find that the most frequently occurring molecular configurations afford superior electronic coupling due to the consistent presence of a single water molecule hydrogen-bonded between the donor and acceptor sites. We attribute the persistence of this water bridge to a ``molecular breakwater'' composed of several hydrophobic residues surrounding the acceptor site. The breakwater supports the function of solvent-organizing residues by limiting the exchange of water molecules between the sterically constrained ET region and the surrounding bulk. When the breakwater is affected by a mutation, bulk solvent molecules disrupt the water bridge, resulting in reduced electronic coupling. These results suggest that protein surface residues may stabilize interprotein solvent dynamics to enable coherent ET along a single molecular pathway.