Geometric trade-off between contractile force and fluid drag determines the motility of actomyosin droplets

The actomyosin cytoskeleton, composed of actin filaments (F-actin) and myosin motors, plays pivotal roles in cellular force generation. One of the distinctive abilities of migratory cells is force transmission: intracellularly generated forces are transmitted to the external environments such as extracellular matrices, by which the cell body is propelled forward. Although much is known about biomolecules involved in cell migration, less is known about physical determinants enabling efficient force transmission. This is because the inherent complexities of cells, such as complex actin-membrane interactions, obscure the mechanical contributions of contractile actomyosin networks to force transmission.

To decouple the mechanics from biochemical regulations, here we develop an in vitro biomimetic migratory cell model by encapsulating actomyosin networks into water-in-oil droplets covered with a lipid monolayer [1]. By implementing a cell-like polarization through actin-membrane binding, a polarized actin flow is induced, which generates sliding friction force at the droplet-substrate interface and propels the droplet. Combining microfluidic experiments and active gel theory, we find that a geometric balance between sliding friction force and fluid drag determines the migration speed under substrate confinement. Together, these findings provide a basic physical understanding of actomyosin-based motility controlled through actin flow-induced friction and environmental geometry.