Force Propagation in Active Cytoskeletal Networks

Abstract

In biological systems, molecular-scale forces and motions are pivotal for enabling processes like motility, shape change, and replication. These forces and motions are organized, amplified, and transmitted across macroscopic scales by active materials such as the cytoskeleton, which drives micron-scale cellular movement and re-organization. Despite the integral role of active materials, understanding how molecular-scale interactions alter macroscopic structure and force propagation remains elusive. This knowledge gap presents challenges to the harnessing and regulation of such dynamics across diverse length scales. Here, we demonstrate how mediating the bundling of microtubules can shift active matter between a global force-transmitting phase and a local force-dissipating phase. A fivefold increase in microtubule effective length results in the transition from local to global phase with a hundredfold increase in velocity autocorrelation. Through theory and simulation, we identify signatures of a percolation-driven transition between the two phases. This provides evidence for how force propagation can be generated when local molecular interactions reach a sufficient length scale. We show that force propagation in the active matter system enables material transport. Consequently, we demonstrate that the global phase is capable of facilitating millimeter-scale human cell transport and manipulation, as well as powering the movement of aqueous droplets. These findings underscore the potential for designing active materials capable of force organization and transmission. Our results lay the foundation for further exploration into the organization and propagation of forces/stresses in biological systems, thereby paving the way for the engineering of active materials in synthetic biology and soft robotics.