(319h) Emergent Micro-Mechanics of Active Bio-Synthetic Composites

The cell cytoskeleton is a composite of protein filaments, including actin, microtubules and intermediate filaments, as well as their associated crosslinking proteins, that is pushed out-of-equilibrium by molecular motors to mediate wide-ranging processes from migration to morphogenesis. The cytoskeleton is, thus, paradigmatic active matter and its composite nature is one of its hallmarks. Yet, state-of-the-art active matter focuses on single force-generating components and substrates. Here, we engineer programmable composites of actin filaments and microtubules that can be versatilely crosslinked and driven by dual motors, kinesin and myosin, to contract, flow, and restructure into diverse morphologies, ranging from interpenetrating scaffolds to phase-separated clusters. We couple optical tweezers microrheology with differential dynamic microscopy and particle-image-velocimetry to demonstrate that composites exhibit emergent rheological properties that arise from cooperativity between actin and microtubules as well as competition between myosin and kinesin. Microtubules confer enhanced force resistance, elastic memory, and ordered dynamics to myosin-driven actin networks, while kinesin and myosin motors compete to delay composite restructuring and suppress de-mixing. Moreover, we find that the nonlinear force response of active composites exhibits emergent high-strength and multi-modal stiffening at intermediate kinesin concentrations and strain rates that vanish at the low and high limits. To couple these emergent non-equilibrium properties with the resilience and strength of synthetic materials, with an eye towards functional materials applications, we incorporate microscale hydrogel inclusions into the composites. We find that the forces that the composites generate are sufficient to flatten, compress, and asymmetrically deform the hydrogels, which, in turn, reinforce, restructure, and prolong the lifetime and percolation of the composites. At the same time, we demonstrate that the deformation profiles of the inclusions can be used as in situ force sensors. Our composite designs, along with our robust microscale rheological measurements, offer a powerful platform for active matter interrogation and discovery, and may prove foundational for diverse materials applications from wound-healing to soft-robotics.