Flagella-like beating of actin bundles driven by self-organized myosin waves

Nat Phys. 2022 Oct;18(10):1240-1247. doi: 10.1038/s41567-022-01688-8. Epub 2022 Aug 8.

Abstract

Wave-like beating of eukaryotic cilia and flagella-threadlike protrusions found in many cells and microorganisms-is a classic example of spontaneous mechanical oscillations in biology. This type of self-organized active matter raises the question of the coordination mechanism between molecular motor activity and cytoskeletal filament bending. Here we show that in the presence of myosin motors, polymerizing actin filaments self-assemble into polar bundles that exhibit wave-like beating. Importantly, filament beating is associated with myosin density waves initiated at twice the frequency of the actin-bending waves. A theoretical description based on curvature control of motor binding to the filaments and of motor activity explains our observations in a regime of high internal friction. Overall, our results indicate that the binding of myosin to actin depends on the actin bundle shape, providing a feedback mechanism between the myosin activity and filament deformations for the self-organization of large motor filament assemblies.