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

Self-Organized criticality (SOC) is characterized by cascading dissipative events observed across diverse natural phenomena, including earthquakes, avalanches, and landslides. During complex physical behaviors of the cell such as migration and division, the F-actin cytoskeleton undergoes dramatic changes in structure, organization, and dynamics, suggestive of large dissipative events. To drive these changes, non-equilibrium activities of molecular motors impart mechanical stresses upon the cytoskeleton. To explore criticality in the dynamics of the cytoskeleton, we reconstruct an experimental model of the cytoskeleton in vitro, composed of purified protein polymers (F-actin), motors (myosin II), and nucleating promoting factors (NPFs). We alter the connectivity and nematic order of F-actin networks through varying NPF concentrations. In ordered (nematic) and poorly percolated networks, dissipative events are exponentially distributed. By contrast, in disordered (branched) and highly percolated networks, dissipative events are Levy- distributed and exhibit 1/f noise, characteristic to SOC. The increased disorder attenuates the propagation of stress, distributes it amongst stiffer eigenmodes, and localizes it spatially, reminiscent of strong localization of electromagnetic waves in disordered lattices. Finally, the extent of disorder determines the magnitude of mechanical stress applied, as it influences the size and activity of myosin II filaments, demonstrating that SOC is regulated by chemical-mechanical feedback.