Elucidating Chiral Myosin-Induced Actin Dynamics: From Single Filament Behavior to Collective Structures

The myosin superfamily comprises over 70 classes, each with multiple subclasses, and shows substantial diversity in properties such as velocity, ATPase activity, duty ratio, and directionality. This functional diversity underpins the specialized roles of each myosin in various organisms, organs, and cell types. Recent studies have revealed that certain myosins induce chiral curved motions of actin filaments. However, this newly identified property remains largely unexplored. Here, we investigated this chiral motion in vitro using Chara corallina myosin XI ( Cc XI), which drives fast counterclockwise (CCW) movement of actin filaments. This chiral motion arises from asymmetric displacement at the filament’s leading tip, and its curvature depends on the surface density of myosin. Surprisingly, at near-physiological actin concentrations, actin filaments exhibiting chiral curved motion undergo collective motion, spontaneously forming a novel structure— termed the actin chiral ring (ACR)—that exhibits persistent CCW rotation. ACRs display remarkable stability, continuing to rotate at their formation site until ATP is depleted, while maintaining their structure even after rotation ceases. This stability is unprecedented among reported collective motions of cytoskeletal proteins driven by various motors. Our findings demonstrate that myosins with chiral activity can autonomously organize actin filaments into stable, chiral structures through collective dynamics, providing new insights into actin self-organization by unconventional myosins. This study advances our understanding of the diverse functional roles of unconventional myosins and introduces a new paradigm for cytoskeletal organization.