Nonlinear local straining leads to non-equilibrium deformation fields and dynamics of motor-driven cytoskeleton composites

The cytoskeleton continuously self-generates forces and reconfigures itself – in part by motor proteins pushing and pulling on the comprising filaments – to enable diverse mechanical responses to local stresses and strains. We previously showed that actin-microtubule composites, driven by motor proteins can restructure into variety of morphologies from interpenetrating filamentous networks to de-mixed amorphous clusters. Here we combine optical tweezer microrheology, fluorescence microscopy and differential dynamic microscopy (DDM) to characterize the stress response and deformation field of composites undergoing local cyclic straining. We use space- and time-resolved DDM (str-DDM) to quantify the time-varying filament deformations and stress propagation and characterize the effects of motor concentration and strain rate on the dynamics and stress propagation. We show that intermediate concentrations of kinesin motors lead to the most pronounced strain alignment and stress propagation while both low and high motor concentrations lead to a more rapidly decaying response. Composite dynamics also exhibit similar emergent non-monotonic dependencies on strain speed owing to the different relaxation mechanisms available to structurally-evolving composites.