F-actin architecture governs self-organized criticality in the cytoskeleton

Self-Organized criticality (SOC) is observed across diverse natural phenomena, including earthquakes, avalanches, and landslides. Signatures of critical phenomena include fractal geometry, 1/f noise, and power-law distributed dissipative events. Recent work has suggested that living systems are poised close to critical points. For example, cells quickly change their shape, and dramatically remodel their internal organization during cell migration or cell division, suggestive of critical behavior in their internal mechanical machinery, the cell cytoskeleton. Composed of protein polymers and mechano-chemical enzymes, ‘active’ stresses are imparted by the enzymes to the polymer network, which accumulate from the molecular scale to the scale of the cell. 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) and enzymes (myosin II), whose organization and activity are controlled precisely. Upon initiation of myosin II activity within F-actin, the network becomes highly dynamic. If the F-actin network is branched, dissipative events are Levy-α distributed and exhibit 1/f noise. By contrast, if the F-actin network is bundled, dissipative events follow double exponential tails. Thus, cells can control their F-actin organization from fractal-like branches to linear bundles to control their approach to criticality, and utilize power-law dissipative events to dramatically remodel their cytoskeleton and ultimately change shape.