Feedback between F-actin organization and active stress governs criticality and energy localization in the cell cytoskeleton

Abstract

Self-organized criticality can occur in earthquakes, avalanches and biological processes, and is characterized by intermittent, scale-free energy dissipation. In living cells, the actin cytoskeleton undergoes dynamic structural reorganization, particularly during migration and division, where molecular motors generate mechanical stresses that drive large dissipative events. However, the mechanisms governing these critical transitions remain unclear. Here we show that cytoskeletal criticality emerges from the interplay between F-actin organization and active stress generation. Our study focuses on a minimal actomyosin system in vitro, which is composed of F-actin filaments, myosin II motors and nucleation-promoting factors. By systematically varying the actin connectivity and nematic order, we demonstrate that ordered and sparsely connected networks exhibit exponential stress dissipation, whereas disordered and highly connected networks show heavy-tailed distributions of energy release and the 1/f noise characteristic of self-organized criticality. Increased disorder leads to stress localization, shifting force propagation into stiffer mechanical modes, reminiscent of Anderson localization in condensed-matter systems. Furthermore, we show that network architecture directly regulates the myosin II filament size, establishing a chemical–mechanical feedback loop that modulates criticality. Our findings provide insights into the collective cytoskeletal dynamics, energy localization and cellular self-organization.