Ambient Fluid Rheology Modulates Oscillatory Instabilities in Filament-Motor Systems

Abstract

Semi-flexible filaments interacting with molecular motors and immersed in rheologically complex and viscoelastic media constitute a common motif in biology. Synthetic mimics of filament-motor systems also feature active or field-activated filaments. A feature common to these active assemblies is the spontaneous emergence of stable oscillations as a collective dynamic response. In nature, the frequency of these emergent oscillations is seen to depend strongly on the viscoelastic characteristics of the ambient medium. Motivated by these observations, we study the instabilities and dynamics of a minimal filament-motor system immersed in model viscoelastic fluids. Using a combination of linear stability analysis and full non-linear numerical solutions, we identify steady states, test the linear stability of these states, derive analytical stability boundaries, and investigate emergent oscillatory solutions. We show that the interplay between motor activity, filament and motor elasticity, and fluid viscoelasticity allows for stable oscillations or limit cycles to bifurcate from steady states. When the ambient fluid is Newtonian, frequencies are controlled by motor kinetics at low viscosities, but decay monotonically with viscosity at high viscosities. In viscoelastic fluids that have the same viscosity as the Newtonian fluid, but additionally allow for elastic energy storage, emergent limit cycles are associated with higher frequencies. The increase in frequency depends on the competition between fluid relaxation time-scales and time-scales associated with motor binding and unbinding. Our results suggest that both the stability and oscillatory properties of active systems may be controlled by tailoring the rheological properties and relaxation times of ambient fluidic environments.