DNA double helix, a tiny electromotor

Christopher Maffeo, Lauren Quednau, James Wilson, and Aleksei Aksimentiev
Nature Nanotechnology 18 238-242 (2023)
DOI:10.1038/s41565-022-01285-z  BibTex

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Human civilization runs on rotary motors, from cars to planes, from conveyer belts to power generators, from pumps to ice cream mixers. Surprisingly, very few examples of rotary motors exist at the nanoscale. FoF1 ATP synthase transforms the energy of electrochemical gradient to power a cycle of catalytic reactions to synthesize the universal energy carrier, ATP. The flagellum motor uses the electrochemical gradient to spin a polymer filament that propels a bacterium in water. However, the physical mechanism utilized by these biological motors—diffusion biased by chemical reactions—is fundamentally different from the mechanisms utilized in macroscopic man-made machines. Is it really not possible to construct a nanoscale system that directly convert flux into thrust and, perhaps, do that using electric field as an energy source?

In this report we describe one such system, a molecule of DNA. In addition to carrying  hereditary genetic information, DNA is well known for its eye catching double helical shape, the shape of a screw. While a helix is a not an uncommon shape among biological polymers, the high electric charge of the DNA makes it uniquely suitable to act as an electromotor. When placed in electrolyte solution, the counter-ions dissolved in the solution will surround the DNA helix, neutralizing its charge. Subject to electric field, the counter ions will flow pass the molecule, dragging the fluid along, a phenomenon known as the electro-osmotic flow. But will that flow be sufficient to impart torque on the molecule given the granularity of the solution, the unchartered viscosity of the fluid within the DNA groves and substantial thermal fluctuations omnipresent at the nanoscale?

To answer this question we performed state-of-the-art all-atom molecular dynamics simulations that are capable of resolving the behavior of individual atoms in both the DNA molecule and the surrounding solvent. We show that, subject to a modest electric field, the DNA molecule rotates billions of revolutions per minute, with the rotation direction prescribed by its helicity. Using double stranded RNA as a control, we show how the rotation speed depends on the parameters of the helix and demonstrate that the rotation is driven by direct momentum transfer from the fluid flow to the helix, just like in man-made macroscopic machines. Further, we show that a single DNA duplex can generate substantial torque, on par with that of an ATP synthase, when placed in a nanopore in a thin membrane, and that that torque is sufficient to power rotation of much larger spherical and rod-shape loads, opening the possibility of using DNA for the construction of nanoscale  electromotors.

Abstract

Flowing fluid past chiral objects has been used for centuries to power rotary motion in man-made machines. By contrast, rotary motion in nanoscale biological or chemical systems is produced by biasing Brownian motion through cyclic chemical reactions. Here we show that a chiral biological molecule, a DNA or RNA duplex rotates unidirectionally at billions of revolutions per minute when an electric field is applied along the duplex, with the rotation direction being determined by the chirality of the duplex. The rotation is found to be powered by the drag force of the electro-osmotic flow, realizing the operating principle of a macroscopic turbine at the nanoscale. The resulting torques are sufficient to power rotation of nanoscale beads and rods, offering an engineering principle for constructing nanoscale systems powered by electric field.