A nanoscale reciprocating rotary mechanism with coordinated mobility control.

Eva Bertosin, Christopher M. Maffeo, Thomas Drexler, Maximilian N. Honemann, Aleksei Aksimentiev, and Hendrik Dietz
Nature Communications 12(1) 7138 (2021)
DOI:10.1038/s41467-021-27230-7  PMID:34880226  BibTex


In collaboration with the Dietz laboratory, we created and characterized a nanoscale rotary object, the first of its kind, that couples large scale mechanical transitions of the stator with rotation of the shaft. The rotary object was made using DNA origami with several interlocking parts that iterative design guided by experimental cryo-EM reconstructions and MD simulations. Experiments revealed that the shaft rotates randomly, dwelling at intervals spaced 120 degrees, which matches the three-fold pseudo-symmetry of the stator. Simulations characterized the conformation and dynamics of multiple rotary assembly designs, and revealed how the cam in the rotary shaft and the stator conformation are coupled. This study represents a breakthrough in the design and fabrication of nanoscale rotary systems, bringing macroscopic mechanical principles to a microscopic world.


Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions. Mechanical deformation can be surprisingly efficient in realizing such coupling, as demonstrated by the FoF1 ATP synthase. Here, we describe a synthetic molecular mechanism that transforms a rotary motion of an asymmetric camshaft into reciprocating large-scale transitions in a surrounding stator orchestrated by mechanical deformation. We design the mechanism using DNA origami, characterize its structure via cryo-electron microscopy, and examine its dynamic behavior using single-particle fluorescence microscopy and molecular dynamics simulations. While the camshaft can rotate inside the stator by diffusion, the stator's mechanics makes the camshaft pause at preferred orientations. By changing the stator's mechanical stiffness, we accelerate or suppress the Brownian rotation, demonstrating an allosteric coupling between the camshaft and the stator. Our mechanism provides a framework for manufacturing artificial nanomachines that function because of coordinated movements of their components.

Equilibration simulation of six rotary assembly design variants created with different designed stator (blue, green and orange) stiffnesses. Stiffer stators resulted in rotation at a reduced rate and, if sufficiently stiff, supressed rotation.

Driven rotation of three of the design variants. Rotation was driven using a custom steered molecular dynamics potential to move the cam relative to the stator at a constant rate.

Average conformation of the rotary assemblies after binning conformations taken from the driven rotation simulations using 30 degree increments, and averaging within each bin. The animation plays through all twelve bins.