Mechanism underlying the ultralow energy-consumption rapid ion dehydration for the high flux of KcsA potassium channels

Abstract

High-flux and ultralow energy consumption (UEC) transport of biological and artificial ion channels has been widely reported [1-22]. However, there is a precondition for such transport: UEC rapid ion dehydration, which underlying mechanism is a remaining challenge. Here, by molecular dynamics (MD) simulations, we demonstrate that a K+ ion can transfer from the hydration water outside KcsA channel to the bound water in the channel without its hydration water accompanying, i.e., a tunneling-like motion, which provides a basis for the UEC dehydration of ions. In our simulations, a KcsA channel was divided into three regions: Cavity-1, Cavity-2 and the filter. As a K+ ion moves from Cavity-1 to Cavity-2, there occurs a resonant energy transfer to the ion from the filter-confined coherently oscillating ions, leading to a tunneling-like motion of the ion from the Cavity-1 to Cavity-2 water with no hydration shell accompanying and no influence on the Cavity-2 water. As the K+ ion further moves from Cavity-2 to the filter, the ion adjusts its hydration-shell water structure to coherence-resonantly couples with the filter-confined ions, leading to another tunneling-like motion to reach complete dehydration. These two consecutive processes constitute a "resonant tunneling" of the ion from Cavity-1 to the filter, as a basis for the UEC rapid dehydration. Our findings provide an understanding of the dehydration dynamics in biological channels and its relationship with the UEC high-flux, potentially promoting the development of artificial membranes design.