DNA Gold Nanoparticle Motors Demonstrate Processive Motion with Bursts of Speed Up to 50 nm Per Second

Abstract

Synthetic motors that consume chemical energy to produce mechanical work offer potential applications in many fields that span from computing to drug delivery and diagnostics. Among the various synthetic motors studied thus far, DNA-based machines offer the greatest programmability and have shown the ability to translocate micrometer-distances in an autonomous manner. DNA motors move by employing a burnt-bridge Brownian ratchet mechanism, where the DNA "legs" hybridize and then destroy complementary nucleic acids immobilized on a surface. We have previously shown that highly multivalent DNA motors that roll offer improved performance compared to bipedal walkers. Here, we use DNAgold nanoparticle conjugates to investigate and enhance DNA nanomotor performance. Specifically, we tune structural parameters such as DNA leg density, leg span, and nanoparticle anisotropy as well as buffer conditions to enhance motor performance. Both modeling and experiments demonstrate that increasing DNA leg density boosts the speed and processivity of motors, whereas DNA leg span increases processivity and directionality. By taking advantage of label-free imaging of nanomotors, we also uncover Levy-type motion where motors exhibit bursts of translocation that are punctuated with transient stalling. Dimerized particles also demonstrate more ballistic trajectories confirming a rolling mechanism. Our work shows the fundamental properties that control DNA motor performance and demonstrates optimized motors that can travel multiple micrometers within minutes with speeds of up to 50 nm/s. The performance of these nanoscale motors approaches that of motor proteins that travel at speeds of 100−1000 nm/s, and hence this work can be important in developing protocellular systems as well next generation sensors and diagnostics.

Functional DNA-based cytoskeletons for synthetic cells

“…They were functionalized with cholesterol-tagged DNA and attached to the filaments by means of complementary base-pairing with multiple RNA overhangs on the filaments. We propose that the guided directional movement of the vesicle is based on a burnt-bridge mechanism 30 – 33 . On addition of RNase H, which selectively cleaves RNA in DNA–RNA hybrids, the hybridized RNA is hydrolysed.…”

An Artificial Protein-Based Burnt-Bridges Molecular Motor Design

“…This latter model demonstrated the importance of balancing chemical kinetic rates of multiple interacting tethers with the timescale of bead diffusion. Interestingly, saltatory dynamics have not been observed in monowheel-like designs implementing nanoscale hubs [38,46], demonstrating the role that polyvalency can have in influencing motility [47][48][49].…”

“…The peptides provided as substrates in these LM experiments bridge a fluorophore and quencher, whereby peptide cleavage releases the quencher to solution and the surface-bound products become fluorescent. In the current experiments, we used bright-field microscopy only, to track the dynamics of the LM, but the system is adaptable to fluorescence-based measurements as has been done to image the track generated by DNA-based polyvalent BBR designs [12,38,46].…”

Chemically modified nucleic acids and DNA intercalators as tools for nanoparticle assembly

“…Employing click chemistry to make stable nanoparticle dimers is of broad interest and it has been recently applied in the fabrication and study of nanoparticle motors on surfaces. Recently, Bazrafshan et al 103 reported the fastest DNA–gold nanoparticles nanomotors to date, by optimising enzyme and buffer conditions as well as DNA leg span and density. To test whether their nanomotors moved by a rolling motion, they utilised copper-free click chemistry to ligate DNA-coated 50 nm gold nanoparticle to form motor dimers.…”

“…These dimers demonstrated that nanoparticles motors generated ballistic trajectories, hence they moved predominantly by a rolling mechanism. 103 …”