Highly Polyvalent DNA Motors Generate 100+ pN of Force via Autochemophoresis

Motor proteins such as myosin, kinesin, and dynein are essential to eukaryotic life and power countless processes including muscle contraction, wound closure, cargo transport, and cell division. The design of synthetic nanomachines that can reproduce the functions of these motors is a longstanding goal in the field of nanotechnology. DNA walkers, which are programmed to "walk" along defined tracks via the burnt bridge Brownian ratchet mechanism, are among the most promising synthetic mimics of these motor proteins. While these DNA-based motors can perform useful tasks such as cargo transport, they have not been shown to be capable of cooperating to generate large collective forces for tasks akin to muscle contraction. In this work, we demonstrate that highly polyvalent DNA motors (HPDMs), which can be viewed as cooperative teams of thousands of DNA walkers attached to a microsphere, can generate and sustain substantial forces in the 100+ pN regime. Specifically, we show that HPDMs can generate forces that can unzip and shear DNA duplexes (∼12 and ∼50 pN, respectively) and rupture biotin-streptavidin bonds (∼100-150 pN). To help explain these results, we present a variant of the burnt-bridge Brownian ratchet mechanism that we term autochemophoresis, wherein many individual force generating units generate a self-propagating chemomechanical gradient that produces large collective forces. In addition, we demonstrate the potential of this work to impact future engineering applications by harnessing HPDM autochemophoresis to deposit "molecular ink" via mechanical bond rupture. This work expands the capabilities of synthetic DNA motors to mimic the force-generating functions of biological motors. Our work also builds upon previous observations of autochemophoresis in bacterial transport processes, indicating that autochemophoresis may be a fundamental mechanism of pN-scale force generation in living systems.