Polarity sorting of actin filaments by motor-driven cargo transport

During the active transport of cellular cargo, forces generated by cargo-associated molecular motors propel the cargo along cytoskeletal tracks. However, the forces impact not only the cargo, but also the underlying cytoskeletal filaments. To better understand the interplay between cargo transport and the organization of cytoskeletal filaments, we employ coarse- grained computer simulations to study actin filaments interacting with cargo-anchored myosin motors in a confined domain. We show that cargo transport can lead to the segregation of filaments into domains of preferred filament polarity separated by clusters of aggregated cargoes. The formation of polarity-sorted filament domains is enhanced by larger numbers of cargoes, more motors per cargo, and longer filaments. Analysis of individual trajectories reveals dynamic and heterogeneous behavior, including locally stable aggregates of cargoes that undergo rapid coalescence into larger clusters when sufficiently close. Our results provide insight into the impact of motor-driven organelle transport on actin filaments, which is relevant both in cells and in synthetic environments. SIGNIFICANCE The actin cytoskeleton is vital for intracellular transport, and there is an intricate interplay between the organization of the actin network and cargo transport by molecular motors. In this work, we use computer simulations to demonstrate that the transport of cargoes by teams of molecular motors can lead to the emergence of filament domains, separated by clusters of cargoes, that are sorted by the polarity of filaments. The results, which highlight feedback between transport and filament organization, provide insight into mechanisms influencing the cytoskeleton in cells and in reconstituted systems.