Artificial DNA-nano/microparticle motors: Factors governing speed, run length, and unidirectionality revealed by...

DNA-nano/microparticle motors are burnt-bridge Brownian ratchets (BBR) moving on an RNA-modified two-dimensional surface driven by Ribonuclease H (RNase H), and are one of the fastest artificial molecular motors. Interestingly, these motors with moderate GC contents show processive rolling motion with a characteristic speed of ∼30 nm s^-1 irrespective of particle size ranging from 100 to 5000 nm, whereas run length increases with particle size. Here we performed geometry-based kinetic simulations of DNA-nano/microparticle motors with the sizes of 100, 500, 1000, and 5000 nm to identify factors governing speed, run length, and unidirectionality. The simulations reproduced experimental trends: run length and unidirectionality increased with particle size, whereas median speed varied within a relatively narrow range of 20-50 nm s^-1. This weak particle-size dependence of speed was caused by a trade-off between step size and pause length, both of which increased with particle size. In contrast, the run length and the unidirectionality increased with the particle size because large particles had high multivalency which suppresses stochastic detachment of the motor, high RNA hydrolysis efficiency under the motor trajectory which realizes almost perfect BBR motion, and stepping direction highly biased to forward. For all particle sizes examined, the speed increased from ∼20-30 to ∼220-250 nm s^-1 by 10-fold increases in DNA/RNA hybridization, RNase H binding, and RNA hydrolysis rates (from 0.8 to 8.0, 7.2 to 72, and 3.0 to 30 s^-1, respectively), even when considering the rotational diffusion of these particles. However, for the largest 5000-nm motor, the duration of rotational diffusion (∼0.04 s) reached ∼13% of the pause length (∼0.30 s) under the fast kinetic condition, decreasing the median speed from 250 to 220 nm s^-1. Our results indicate that small DNA-particle motors have a potential for further acceleration because the contribution of rotational diffusion remains small.