Abstract

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 F1FO 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.

Highlights

  • Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions

  • The F1 motor of F1FO ATP synthase is reversible[4,5]: it can either function as a rotary motor powered by the chemical energy of ATP hydrolysis or it can use the mechanical energy of the central shaft rotation to catalyze synthesis of ATP

  • We presented a compliant nanoscale rotary mechanism with a central camshaft surrounded by a stator with programmable stiffness

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Summary

Introduction

Biological molecular motors transform chemical energy into mechanical work by coupling cyclic catalytic reactions to large-scale structural transitions. The F1 motor of F1FO ATP synthase is reversible[4,5]: it can either function as a rotary motor powered by the chemical energy of ATP hydrolysis or it can use the mechanical energy of the central shaft rotation to catalyze synthesis of ATP. We describe the construction, computational characterization and experimental validation of a rotary mechanism with user-defined power and motion transmission We conceive this object by combining macroscale machine design concepts with functional and structural aspects of the ATP synthase, and consider it to be a stepping stone toward creating artificial machines that achieve and generalize functionalities observed in biological motors

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