Molecular propulsion: chemical sensing and chemotaxis of DNA driven by RNA polymerase

Abstract

Living cells sense extracellular signals and direct their movements in response to stimuli in environment. Such autonomous movement allows these machines to sample chemical change over a distance, leading to chemotaxis. Synthetic catalytic rods have been reported to chemotax toward hydrogen peroxide fuel. Nevertheless individualized autonomous control of movement of a population of biomolecules under physiological conditions has not been demonstrated. Here we show the first experimental evidence that a molecular complex consisting of a DNA template and associating RNA polymerases (RNAPs) displays chemokinetic motion driven by transcription substrates nucleoside triphosphates (NTPs). Furthermore this molecular complex exhibits a biased migration into a concentration gradient of NTPs, resembling chemotaxis. We describe this behavior as "Molecular Propulsion", in which RNAP transcriptional actions deform DNA template conformation engendering measurable enhancement of motility. Our results provide new opportunities for designing and directing nanomachines by imposing external triggers within an experimental system.

Figure 1

FRAP measurement of chemokinesis by T7 RNAP transcription. Error bar: standard deviation. Percentage increase in the apparent diffusion coefficient compared to Brownian diffusion is shown.

Figure 2

Dependence of diffusivity on elongation and initiation: comparison with runoff transcription. Percentage difference of diffusion coefficient compared to the runoff transcription within each set is noted. Error bar: standard deviation.

Figure 3

DNA chemotaxis: biased DNA transport toward NTP gradient. Error bar: range. Bias [normalized, (F_NTP - F_control)/F_control; purple line] reveals enhanced DNA transport toward the NTP gradient, demonstrating DNA chemotaxis mediated by transcription.