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Sustained unidirectional rotation of a self-organized DNA rotor on a nanopore

Abstract

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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Fig. 1: DNA rotor on a solid-state nanopore.
Fig. 2: Unidirectional rotation of a DNA rotor under a transmembrane voltage.
Fig. 3: DNA rotors are deformed by the E-field and driven to rotation by the flow.
Fig. 4: Unidirectional rotation of rotors driven by a transmembrane salt gradient.

Data availability

All experimental data are available at https://doi.org/10.5281/zenodo.6513594.

Code availability

MATLAB codes for data processing are available at https://doi.org/10.5281/zenodo.6513594. Julia codes used for numerical simulation are available at https://gitlab.gwdg.de/LMP-pub/nanoturbines.

References

  1. Yoshida, M., Muneyuki, E. & Hisabori, T. ATP synthase—a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2, 669–677 (2001).

    Article  Google Scholar 

  2. Srivastava, A. P. et al. High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane. Science 360, eaas9699 (2018).

    Article  Google Scholar 

  3. Minamino, T., Imada, K. & Namba, K. Molecular motors of the bacterial flagella. Curr. Opin. Struct. Biol. 18, 693–701 (2008).

    Article  Google Scholar 

  4. Perkins, G. et al. Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J. Struct. Biol. 119, 260–272 (1997).

    Article  Google Scholar 

  5. Ramezani, H. & Dietz, H. Building machines with DNA molecules. Nat. Rev. Genet. 21, 5–26 (2020).

    Article  Google Scholar 

  6. Ozin, G. A., Manners, I., Fournier‐Bidoz, S. & Arsenault, A. Dream nanomachines. Adv. Mater. 17, 3011–3018 (2005).

    Article  Google Scholar 

  7. Browne, W. & Feringa, B. Making molecular machines work. Nat. Nanotechnol. 1, 25–35 (2006).

    ADS  Article  Google Scholar 

  8. Astumian, R. D. Thermodynamics and kinetics of a Brownian motor. Science 276, 917–922 (1997).

    Article  Google Scholar 

  9. Feynman, R. There’s plenty of room at the bottom: an invitation to open up a new field of physics. Eng. Sci. 23, 22–36 (1960).

    Google Scholar 

  10. Brown, A. I. & Sivak, D. A. Theory of nonequilibrium free energy transduction by molecular machines. Chem. Rev. 120, 434–459 (2019).

    Article  Google Scholar 

  11. Stoddart, J. F. The chemistry of the mechanical bond. Chem. Soc. Rev. 38, 1802–1820 (2009).

    Article  Google Scholar 

  12. García-López, V., Liu, D. & Tour, J. M. Light-activated organic molecular motors and their applications. Chem. Rev. 120, 79–124 (2019).

    Article  Google Scholar 

  13. Kopperger, E. et al. A self-assembled nanoscale robotic arm controlled by electric fields. Science 359, 296–301 (2018).

    ADS  Article  Google Scholar 

  14. Thubagere, A. J. et al. A cargo-sorting DNA robot. Science 357, eaan6558 (2017).

    Article  Google Scholar 

  15. Soong, R. K. et al. Powering an inorganic nanodevice with a biomolecular motor. Science 290, 1555–1558 (2000).

    ADS  Article  Google Scholar 

  16. Yehl, K. et al. High-speed DNA-based rolling motors powered by RNase H. Nat. Nanotechnol. 11, 184–190 (2016).

    ADS  Article  Google Scholar 

  17. Golestanian, R. Synthetic mechanochemical molecular swimmer. Phys. Rev. Lett. 105, 018103 (2010).

    ADS  Article  Google Scholar 

  18. Douglas, S. M. et al. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 459, 414–418 (2009).

    ADS  Article  Google Scholar 

  19. Van Dorp, S., Keyser, U. F., Dekker, N. H., Dekker, C. & Lemay, S. G. Origin of the electrophoretic force on DNA in solid-state nanopores. Nat. Phys. 5, 347–351 (2009).

    Article  Google Scholar 

  20. Anderson, J. L. Colloid transport by interfacial forces. Annu. Rev. Fluid Mech. 21, 61–99 (1989).

    ADS  Article  Google Scholar 

  21. Golestanian, R. Phoretic active matter. Preprint at https://arxiv.org/abs/1909.03747 (2019).

  22. Castro, C. E., Su, H.-J., Marras, A. E., Zhou, L. & Johnson, J. Mechanical design of DNA nanostructures. Nanoscale 7, 5913–5921 (2015).

    ADS  Article  Google Scholar 

  23. Bergou, M., Wardetzky, M., Robinson, S., Audoly, B. & Grinspun, E. Discrete elastic rods. ACM Trans. Graph 27, 1–12 (2008).

    Article  Google Scholar 

  24. Lee, C. et al. Osmotic flow through fully permeable nanochannels. Phys. Rev. Lett. 112, 244501 (2014).

    ADS  Article  Google Scholar 

  25. Bonthuis, D. J. & Golestanian, R. Mechanosensitive channel activation by diffusio-osmotic force. Phys. Rev. Lett. 113, 148101 (2014).

    ADS  Article  Google Scholar 

  26. Douglas, S. M. et al. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res. 37, 5001–5006 (2009).

    Article  Google Scholar 

  27. Wagenbauer, K. F. et al. How we make DNA origami. ChemBioChem 18, 1873–1885 (2017).

    Article  Google Scholar 

  28. Verschueren, D. V., Yang, W. & Dekker, C. Lithography-based fabrication of nanopore arrays in freestanding SiN and graphene membranes. Nanotechnology 29, 145302 (2018).

    ADS  Article  Google Scholar 

  29. Janssen, X. J. et al. Rapid manufacturing of low-noise membranes for nanopore sensors by trans-chip illumination lithography. Nanotechnology 23, 475302 (2012).

    Article  Google Scholar 

  30. Churchman, L. S., Ökten, Z., Rock, R. S., Dawson, J. F. & Spudich, J. A. Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proc. Natl Acad. Sci. USA 102, 1419–1423 (2005).

    ADS  Article  Google Scholar 

  31. Kwok, H., Briggs, K. & Tabard-Cossa, V. Nanopore fabrication by controlled dielectric breakdown. PLoS ONE 9, e92880 (2014).

    ADS  Article  Google Scholar 

  32. Ovesný, M., Křížek, P., Borkovec, J., Švindrych, Z. & Hagen, G. M. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30, 2389–2390 (2014).

    Article  Google Scholar 

  33. Lyubchenko, Y. L. & Shlyakhtenko, L. S. AFM for analysis of structure and dynamics of DNA and protein-DNA complexes. Methods 47, 206–213 (2009).

    Article  Google Scholar 

  34. Horcas, I. et al. WSXM: a software for scanning probe microscopy and a tool for nanotechnology. Rev. Sci. Instrum. 78, 013705 (2007).

    ADS  Article  Google Scholar 

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Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Contributions

X.S., D.V., H.D. and C.D. conceived the concept of DNA rotors in nanopores. A.-K.P. and H.D. designed and prepared the DNA origami structures. X.S. designed the nanopore experiment and fabricated nanopore devices. X.S. and W.Z. conducted nanopore experiments. A.M.-G. performed AFM measurements. X.S. and D.V. wrote the data analysis program and analysed data. J.I. and R.G. designed and conducted theoretical modelling and simulations. All authors discussed the experimental findings and co-wrote the manuscript.

Corresponding authors

Correspondence to Ramin Golestanian, Hendrik Dietz or Cees Dekker.

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Nature Physics thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Notes 1–4, Figs. 1–14, Tables 1–5 and captions for Videos 1–6.

Reporting Summary

Supplementary Table

DNA sequences of staple strands

Supplementary Video 1

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).

Supplementary Video 2

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.

Supplementary Video3

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.

Supplementary Video 4

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.

Supplementary Video 5

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.

Supplementary Video 6

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

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