Plugging active "hardware" into biological "software"

The actomyosin cytoskeleton is a naturally occurring active gel, which exhibits a density instability called contraction. This remarkable ability drives a wide range of autonomous mechanical behaviors in cells, allowing them to move, change shape, exert force, sense stiffness, and maintain constant tension. A thorough description of these behaviors requires a quantitative characterization of the mechanical properties of contractile active gels. However, mechanical properties are conventionally expressed as responses to external stresses and strains. Which physical quantities describe the response to molecular motor activity? Although researchers have long known that motors hydrolyze ATP to drive contraction, the relationship between motor activity and contraction remains poorly understood. Here we experimentally measure myosin ATPase activity and actomyosin contractile outputs in gels of reconstituted proteins, and express relationships between these quantities as response functions. Quantifying these response functions allows us to identify optimal operating conditions, such as maximum energy economy and maximum performance. We hypothesize that cells dynamically switch between these distinct optima to adapt to changing mechanical tasks, uncertain environments, and evolutionary pressures. Control over optimal contractile states could also be leveraged in the design of small robots actuated by actomyosin active gels. Finally, the response functions we introduce here are a necessary first step towards future studies which quantify how biochemical feedback loops connect information from contractile outputs back into ATPase input regulation.