# Elucidating chiral myosin–induced actin dynamics: From single-filament behavior to collective structures

## TL;DR

This study shows how certain myosin proteins can cause actin filaments to move in chiral paths and form stable rotating ring structures, revealing a new mechanism for cellular asymmetry.

## Contribution

The discovery that chiral myosin activity can autonomously organize actin into stable rotating ring structures represents a novel mechanism for cytoskeletal self-assembly.

## Key findings

- Chiral myosin induces single actin filaments to move along curved paths.
- Actin filaments form stable rotating ring structures called actin chiral rings (ACRs) at high concentrations.
- ACRs maintain structure and rotation until ATP is depleted, showing unprecedented stability in cytoskeletal collective motion.

## Abstract

Myosins are motor proteins that move along actin filaments and underpin various intracellular functions. Recently, some myosins have been found to drive actin filaments along chiral curved paths, but the mechanisms and significance of this behavior remain largely unexplored. Here, we investigated this activity and found that it not only drives chiral curved motion of single actin filaments but also organizes them into stable, unidirectionally rotating ring structures through collective motion. These rings, termed actin chiral rings (ACRs), spontaneously emerge at high actin concentrations. Our findings uncover a organizing principle of actin self-assembly driven by myosin with chiral activity and provide a framework for understanding how cytoskeletal chirality is established.

The myosin superfamily encompasses over 70 classes, each with multiple subclasses, and exhibits substantial diversity in properties such as velocity, ATPase activity, duty ratio, and directionality. This functional diversity enables the specialized roles of each myosin in various organisms, organs, and cell types. Beyond these well-characterized parameters, a newly recognized property has recently come into focus: Certain myosins drive actin filaments along chiral curved trajectories. However, this newly identified property remains largely unexplored. Here, we investigated this chiral motion in vitro using Chara corallina myosin XI (CcXI), which drives fast clockwise (CW) movement of actin filaments. This chiral motion arises from asymmetric displacement at the filament’s leading tip, and its curvature depends on the myosin density. Surprisingly, at elevated actin concentrations, filaments exhibiting chiral curved motion undergo collective dynamics, spontaneously forming a ring-shaped structure—termed the actin chiral ring (ACR)—that exhibits persistent CW 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 has not been reported 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 motion, providing insights into actin self-organization by unconventional myosins. This paradigm offers a mechanistic basis for how motor-driven molecular asymmetry can give rise to coherent structural chirality at the cellular scale—an essential step in the emergence of cell chirality and asymmetry during development.