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A bio-hybrid DNA rotor–stator nanoengine that moves along predefined tracks

Nature Nanotechnology volume 13, pages 496–503 (2018)Cite this article

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Abstract

Biological motors are highly complex protein assemblies that generate linear or rotary motion, powered by chemical energy. Synthetic motors based on DNA nanostructures, bio-hybrid designs or synthetic organic chemistry have been assembled. However, unidirectionally rotating biomimetic wheel motors with rotor–stator units that consume chemical energy are elusive. Here, we report a bio-hybrid nanoengine consisting of a catalytic stator that unidirectionally rotates an interlocked DNA wheel, powered by NTP hydrolysis. The engine consists of an engineered T7 RNA polymerase (T7RNAP-ZIF) attached to a dsDNA nanoring that is catenated to a rigid rotating dsDNA wheel. The wheel motor produces long, repetitive RNA transcripts that remain attached to the engine and are used to guide its movement along predefined ssDNA tracks arranged on a DNA nanotube. The simplicity of the design renders this walking nanoengine adaptable to other biological nanoarchitectures, facilitating the construction of complex bio-hybrid structures that achieve NTP-driven locomotion.

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Fig. 1: Assembly of the DNA catenane rotary motor.
Fig. 2: Single-molecule FRET studies of the DNA catenane rotatory motor.
Fig. 3: The nanoengine moves along predefined tracks.
Fig. 4: Analysis of the RNA sequential hybridization to iSteps during RCT of the catenane walker.
Fig. 5: Kinetics of nanoengine walking on a path with varying distances between steps.

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Acknowledgements

The authors thank K. Rotscheidt, V. Vieberg and D. Keppner for technical assistance, and D. Ackermann, A. Kristofferson and A. Lange for performing preliminary studies. This work was supported by the Alexander von Humboldt Foundation and the European Research Council (ERC Advanced Grant 267173), the Max-Planck Society and the University of Bonn. N.G.W. acknowledges partial funding by Department of Defense grant W911NF-12-1-0420 and NSF grant DMR-1607854. M.F. thanks H. Famulok (1932–2017) for his genuine and encouraging interest in this work.

Authors contributions

M.F. and J.V. developed the concepts of interlocked bio-hybrid nanoengines and the walking principle. J.V. performed and designed, with M.F., most of the included studies. M.F. supervised the research project. N.P., S.D. and N.G.W. planned and performed the single-molecule fluorescence experiments. All authors discussed the experimental results and contributed to writing the manuscript (J.V. and M.F. performed the bulk of the writing).

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  1. Soma Dhakal

    Present address: Department of Chemistry, Virginia Commonwealth University, Richmond, VA, USA

Authors and Affiliations

  1. LIMES Program Unit Chemical Biology & Medicinal Chemistry, c/o Kekulé Institut für Organische Chemie und Biochemie, University of Bonn, Bonn, Germany

    Julián Valero & Michael Famulok

  2. Center of Advanced European Studies and Research (CAESAR), Bonn, Germany

    Julián Valero & Michael Famulok

  3. Single Molecule Analysis Group, Department of Chemistry, University of Michigan, Ann Arbor, MI, USA

    Nibedita Pal, Soma Dhakal & Nils G. Walter

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Correspondence to Michael Famulok.

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Valero, J., Pal, N., Dhakal, S. et al. A bio-hybrid DNA rotor–stator nanoengine that moves along predefined tracks. Nature Nanotech 13, 496–503 (2018). https://doi.org/10.1038/s41565-018-0109-z

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