Mechanical adaptation via non-equilibrium binding kinetics in the cell cytoskeleton

In engineered materials, bond lifetimes shorten under an applied load. By contrast, biological materials such as the cell cytoskeleton also contain bonds that increase their lifetime under stress. These “catch bonds” can break detailed balance at the molecular scale and increase the toughness of passive materials to externally applied stresses. However, the catch bonds found in the cell cytoskeleton are molecular motors that generate stresses internally via ATP hydrolysis. Through coarse-grained molecular dynamics simulations of the actomyosin cytoskeleton, we explore the effect of the resulting feedback between active stresses and force-dependent binding kinetics on large-scale material and thermodynamic properties of active materials. We show that active catch bonds induce a macroscopic fluid-solid transition, where the extent of broken detailed balance and distinct time-reversal symmetries characterize each material phase. Our work illustrates how the combination of non-equilibrium binding and active stresses mounts an adaptive mechanical response in biological materials.