Energy transduction and signal averaging of fluctuating electric fields by a single protein ion channel

Abstract

We demonstrate the electrical rectification and signal averaging of fluctuating signals using a biological nanostructure in aqueous solution: a single protein ion channel inserted in the lipid bilayer characteristic of cell membranes. The conversion of oscillating, zero time-average potentials into directional currents permits charging of a load capacitor to significant steady-state voltages within a few minutes in the case of the outer membrane porin F (OmpF) protein, a bacterial channel of Escherichia coli. The experiments and simulations show signal averaging effects at a more fundamental level than the traditional cell and tissue scales, which are characterized by ensembles of many ion channels operating simultaneously. The results also suggest signal transduction schemes with bio-electronic interfaces and ionic circuits where soft matter nanodiodes can be coupled to conventional electronic elements.

Optimizing Energy Transduction of Fluctuating Signals with Nanofluidic Diodes and Load Capacitors

“…Figure shows the basic scheme for the electrical transduction of a fluctuating signal of zero‐average into a net current that allows charging the load capacitor to significant voltages . The process is experimentally robust and can be scaled up by using multipore membranes instead of single‐nanofluidic diodes .…”

“…The hybrid network can be described theoretically by means of equivalent electrical circuits that permit to simulate the system response for each practical design . We will focus here on the case of polymeric nanopores but the concepts developed can also be implemented using solid‐state pores and ion channels …”

“…Note also that hybrid circuits allow correcting for the mismatch between the electrical characteristics of nanopores and solid‐state elements. Indeed, these systems are mismatched not only in their impedances but also in their operating voltages, especially in the case of biological nanopores (ion channels) whose typical voltages are of the order of kT / e = 27 mV, where k is the Boltzmann constant, T is the absolute temperature, end e is the elementary charge . Figure A shows a recent example concerning the rectification of fluctuating signals with a single protein ion channel (the outer membrane porin F protein, a bacterial channel of Escherichia coli ) in a lipid bilayer.…”

“…The physical approach is based on the efficient transduction between the ionic responses obtained at the micro‐ and nanoscale and the electronic readouts characteristic of the solid‐state elements . In particular, we have demonstrated the conversion of fluctuating zero‐average external potentials into nonzero ionic currents, both in artificial and biological systems. These directional currents eventually produce robust electronic responses in hybrid networks with different interconnectivities submitted to white noise input signals …”

“…The conceptual problem is relevant to electrochemical energy conversion and storage procedures, the quantification of the effects caused by external signals on biological ion channels, the study of the noisy responses characteristic of nanosensors and actuators, and the ion pumping and desalination processes with conical nanopores …”