Dual antagonistic role of motor proteins in fluidizing active networks

Abstract

Cells accomplish diverse functions using the same molecular building blocks, from setting up cytoplasmic flows to generating mechanical forces. In particular, transitions between these non-equilibrium states are triggered by regulating the expression and activity of cytoskeletal proteins. However, how these proteins set the large-scale mechanics of the cytoskeleton and drive such non-equilibrium phase transitions remain poorly understood. Here, we show that a minimal network of biopolymers, molecular motors, and crosslinkers exhibits two distinct emergent behaviors depending on its composition, spontaneously flowing like an active fluid, or buckling like an active solid. Molecular motors play a dual antagonistic role, fluidizing or stiffening the network depending on the ATP concentration. By combining experiments, continuum theory, and chemical kinetics, we identify how to assemble materials with targeted activity and elasticity by setting the concentrations of each component. Active and elastic stresses can be further manipulated in situ by light-induced pulses of motor activity, controlling the solid-to-fluid transition. These results highlight how cytoskeletal stresses regulate the self-organization of living matter and set the foundations for the rational design and control of active materials.