Detailed comparative studies of proton relay in native and chemically modified gramicidin channels provide a unique opportunity to uncover the structural basis of biological proton transport. The function of ion channels hinges on their ability to provide surrogate solvation in narrow pore filters so as to overcome the dielectric barrier presented by biological membranes. In the potassium channel KcsA and in the cation channel gramicidin, permeant selectivity and mobility are determined by the proteinaceous matrix via hydrogen bonding, charge-dipole, and dipole-dipole interactions. In particular, main-chain carbonyl groups in these pore interiors play an essential role in the solvation of alkali ions and of protons. In this study, molecular dynamics simulations reveal how the translocation of H+ is controlled by nanosecond conformational transitions exchanging distorted states of the peptidic backbone in the single-file region of a dioxolane-linked analogue of the gramicidin dinner. These results underline the functional role of channel dynamics and provide a mechanism for the modulation of proton currents by fluctuating dipoles.