Long-Range Conductivity in Proteins Mediated by Aromatic Residues

Single-molecule measurements show that many proteins,
lacking any
redox cofactors, nonetheless exhibit electrical conductance on the
order of a nanosiemen over 10 nm distances, implying that electrons
can transit an entire protein in less than a nanosecond when subject
to a potential difference of less than 1 V. This is puzzling because,
for fast transport (i.e., a free energy barrier of zero), the hopping
rate is determined by the reorganization energy of approximately 0.8
eV, and this sets the time scale of a single hop to at least 1 μs.
Furthermore, the Fermi energies of typical metal electrodes are far
removed from the energies required for sequential oxidation and reduction
of the aromatic residues of the protein, which should further reduce
the hopping current. Here, we combine all-atom molecular dynamics
(MD) simulations of non-redox-active proteins (consensus tetratricopeptide
repeats) with an electron transfer theory to demonstrate a molecular
mechanism that can account for the unexpectedly fast electron transport.
According to our MD simulations, the reorganization energy produced
by the energy shift on charging (the Stokes shift) is close to the
conventional value of 0.8 eV. However, the non-ergodic sampling of
molecular configurations by the protein results in reaction-reorganization
energies, extracted directly from the distribution of the electrostatic
energy fluctuations, that are only ∼0.2 eV, which is small
enough to enable long-range conductivity, without invoking quantum
coherent transport. Using the MD values of the reorganization energies,
we calculate a current decay with distance that is in agreement with
experiment.