The actin cytoskeleton is an active semi-flexible polymer network whose non-equilibrium properties coordinate both stable and contractile behaviors to maintain or change cell shape. While myosin motors drive the actin cytoskeleton out-of-equilibrium, the role of myosin-driven active stresses in the accumulation and dissipation of mechanical energy is unclear. To investigate this, we synthesize an actomyosin material in vitro whose active stress content can tune the network from stable to contractile. Each increment in activity determines a characteristic spectrum of actin filament fluctuations which is used to calculate the total mechanical work and the production of entropy in the material. We find that the balance of work and entropy does not increase monotonically and the entropy production rate is maximized in the non-contractile, stable state of actomyosin. Our study provides evidence that the origins of entropy production and activity-dependent dissipation relate to disorder in the molecular interactions between actin and myosin.

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Active stresses are generated and transmitted throughout diverse F-actin architectures within the cell cytoskeleton, and drive essential behaviors of the cell, from cell division to migration. However, while the impact of F-actin architecture on the transmission of stress is well studied, the role of architecture on the ab initio generation of stresses remains less understood. Here, we assemble F-actin networks in vitro, whose architectures are varied from branched to bundled through F-actin nucleation via Arp2/3 and the formin mDia1. Within these architectures, we track the motions of embedded myosin thick filaments and connect them to the extent of F-actin network deformation. While mDia1-nucleated networks facilitate the accumulation of stress and drive contractility through enhanced actomyosin sliding, branched networks prevent stress accumulation through the inhibited processivity of thick filaments. The reduction in processivity is due to a decrease in translational and rotational motions constrained by the local density and geometry of F-actin.

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Essentially all biology is active and dynamic. Biological entities autonomously sense, compute, and respond using energy-coupled ratchets that can produce force and do work. The cytoskeleton, along with its associated proteins and motors, is a canonical example of biological active matter, which is responsible for cargo transport, cell motility, division, and morphology. Prior work on cytoskeletal active matter systems showed either extensile or contractile dynamics. Here, we demonstrate a cytoskeletal system that can control the direction of the network dynamics to be either extensile, contractile, or static depending on the concentration of filaments or transient crosslinkers through systematic variation of the crosslinker or microtubule concentrations. Based off these new observations and our previously published results, we created a simple one-dimensional model of the interaction of filaments within a bundle. Despite its simplicity, our model recapitulates the observed activities of our experimental system, implying that the dynamics of our finite networks of bundles are driven by the local filament-filament interactions within the bundle. Finally, we show that contractile phases can result in autonomously motile networks that resemble cells. Our experiments and model allow us to gain a deeper understanding of cytoskeletal dynamics and provide a stepping stone for designing active, autonomous systems that could potentially dynamically switch states.