Flow-driven rotary motors such as windmills and water wheels drive functional processes in human society. Although examples of such rotary motors also feature prominently in cell biology, their synthetic construction at the nanoscale has remained challenging. Here we demonstrate flow-driven rotary motion of a self-organized DNA nanostructure that is docked onto a nanopore in a thin solid-state membrane. An elastic DNA bundle self-assembles into a chiral conformation upon phoretic docking onto the solid-state nanopore, and subsequently displays a sustained unidirectional rotary motion of up to 20 rev s−1. The rotors harness energy from a nanoscale water and ion flow that is generated by a static chemical or electrochemical potential gradient in the nanopore, which are established through a salt gradient or applied voltage, respectively. These artificial nanoengines self-organize and operate autonomously in physiological conditions, suggesting ways to constructing energy-transducing motors at nanoscale interfaces.
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All experimental data are available at https://doi.org/10.5281/zenodo.6513594.
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We thank A. Aksimentiev, C. Maffeo, M. Tišma, A. Fragasso and A. Barth for discussions, B. Pradhan for help with the single-molecule fluorescence set-up, N. Klughammer for help with the fabrication of fiducial marker grids for dual-channel fluorescence imaging, and P. Ketterer for initial DNA origami structure designs. We acknowledge funding support by Dutch Research Council NWO grant no. NWO-I680 and the European Research Council Advanced Grant 883684 (C.D.). This work was supported by a European Research Council Consolidator Grant to H.D. (GA no. 724261), the Deutsche Forschungsgemeinschaft through grants provided within the Gottfried-Wilhelm-Leibniz Program (H.D.), and the SFB863 Project ID 111166240 TPA9 (H.D.). The work has received support from the Max Planck School Matter to Life (R.G. and H.D.) and the MaxSynBio Consortium (R.G.), which are jointly funded by the Federal Ministry of Education and Research (BMBF) of Germany and the Max Planck Society.
The authors declare no competing interests.
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Supplementary Notes 1–4, Figs. 1–14, Tables 1–5 and captions for Videos 1–6.
DNA sequences of staple strands
Rotary motion of DNA rotors on nanopores. Top row: raw video of the Cy5 channel of each rotor. Middle row: corresponding single-particle localization results of both ends of the DNA rotors. The position of the current frame is marked as orange and blue dots, and the trajectory of the 10 frames before the current frame is shown as solid lines. The two dots are connected with a red bar. Bottom row: corresponding cumulative angular displacement (𝑡). All plots in the video are synced. The video playback frame rate is 40 fps, which is around 10 times slower than the original data (450–500 fps).
Simulated DNA rotors on nanopores. Top view of a collection of different simulated DNA rotors. The 6hb rods are shown in orange and the rim of the pore in red. All parameters were the same for each panel in this video, except for the initial placement of the 6hb rod (shown in blue) on the nanopore. Simulations that terminated early due to translocation of the rod through the pore are marked by a grey background.
Example (1) of bending configurations in 3D simulations of DNA rods on nanopores. A portion of the membrane is shown in grey, the rim of the pore is highlighted in red, and a 3D rendering of the motion of the DNA rod is displayed.
Example (2) of bending configurations in 3D simulations of DNA rods on nanopores. A portion of the membrane is shown in grey, the rim of the pore is highlighted in red, and a 3D rendering of the motion of the DNA rod is displayed.
Example (3) of bending configurations in 3D simulations of DNA rods on nanopores. A portion of the membrane is shown in grey, the rim of the pore is highlighted in red, and a 3D rendering of the motion of the DNA rod is displayed.
Example (4) of bending configurations in 3D simulations of DNA rods on nanopores. A portion of the membrane is shown in grey, the rim of the pore is highlighted in red, and a 3D rendering of the motion of the DNA rod is displayed.
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Shi, X., Pumm, AK., Isensee, J. et al. Sustained unidirectional rotation of a self-organized DNA rotor on a nanopore. Nat. Phys. (2022). https://doi.org/10.1038/s41567-022-01683-z