Large and reversible myosin-dependent forces in rigidity sensing

Cells sense the rigidity of their environment through localized pinching, which occurs when myosin molecular motors generate contractions within actin filaments anchoring the cell to its surroundings. We present high-resolution experiments performed on these elementary contractile units in cells. Our experimental results challenge the current understanding of molecular motor force generation. Surprisingly, bipolar myosin filaments generate much larger forces per motor than measured in single-molecule experiments. Furthermore, contraction to a fixed distance, followed by relaxation at the same rate, is observed over a wide range of matrix rigidities. Finally, stepwise displacements of the matrix contacts are apparent during both contraction and relaxation. Building on a generic two-state model of molecular motor collections, we interpret these unexpected observations as spontaneously emerging features of a collective motor behaviour. Our approach explains why, in the cellular context, collections of resilient and slow motors contract in a stepwise fashion while collections of weak and fast motors do not. We thus rationalize the specificity of motor contractions implied in rigidity sensing compared to previous in vitro observations.