Evolution of mechanical cooperativity among myosin II motors

Abstract

Significance Myosin II is a molecular motor that generates force and motion in muscle cells. During muscle contraction, many myosin II motors bind to the same actin filament, like people pulling on a rope in a tug-of-war. We study how myosin II motors have evolved to coordinate their actions. We find that a key property of muscle performance is how far a filament slides backward when a motor at the end of its cycle releases. This backsliding is not a property of an individual motor; it depends on the entire multimotor system. We find evidence that myosin II has evolved to minimize this backsliding. These evolutionary trends also explain differences in speed and efficiency observed in muscle tissues across different species. Myosin II is a biomolecular machine that is responsible for muscle contraction. Myosin II motors act cooperatively: during muscle contraction, multiple motors bind to a single actin filament and pull it against an external load, like people pulling on a rope in a tug-of-war. We model the dynamics of actomyosin filaments in order to study the evolution of motor–motor cooperativity. We find that filament backsliding—the distance an actin slides backward when a motor at the end of its cycle releases—is central to the speed and efficiency of muscle contraction. Our model predicts that this backsliding has been reduced through evolutionary adaptations to the motor’s binding propensity, the strength of the motor’s power stroke, and the force dependence of the motor’s release from actin. These properties optimize the collective action of myosin II motors, which is not a simple sum of individual motor actions. The model also shows that these evolutionary variables can explain the speed–efficiency trade-off observed across different muscle tissues. This is an example of how evolution can tune the microscopic properties of individual proteins in order to optimize complex biological functions.