Artificial DNA-nano/microparticle motors: Factors governing speed, run-length, and unidirectionality revealed by geometry-based kinetic simulations

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 show a maximum speed of [~]30 nm s-{superscript 1} irrespective of the particle size ranging from 100 to 5000 nm, whereas the run-length increases with the 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 the factors governing speed, run-length, and unidirectionality. The simulations reproduced the experiments quantitatively, and the speed remained constant while the run-length and the unidirectionality increased with the particle size. The constant speed was caused by a trade-off between the step size and the pause length, both of which increased with the 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 the smaller motors with 100, 500, and 1000 nm particles, the speed increased from 20 to 200 nm s-{superscript 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-{superscript 1}, respectively), even when considering the rotational diffusion of these particles. On the other hand, the speed for the largest motor with 5000 nm particle was limited to 100 nm s-{superscript 1}, because the time required for rolling motion ([~]0.3 s) became comparable to the pause length. Our results indicate that DNA-particle motors must possess a nanoscale body to achieve a speed exceeding 100 nm s-{superscript 1}. SignificanceAutonomous artificial molecular motors have a potential to power nano- and micron-scale actuators and devices, but their performances such as speed, run-length, and unidirectionality are inferior to natural motor proteins. Using geometry-based kinetic simulations, we quantitatively analyzed performance metrics of artificial DNA-nano/microparticle motors which autonomously move on RNA-modified two-dimensional surfaces by a burnt-bridge Brownian ratchet mechanism. Our study revealed the mechanism why their speed is almost independent of the particle size, while the run-length and unidirectionality increases with the particle size. We also identified how multivalent binding, mode of detachment, and rotational diffusion set fundamental limits of the speed, run-length, and unidirectionality. Our results provide a general design strategy for engineering high-performance artificial molecular motors.