Active Microphase Separation in Mixtures of Microtubules and Tip-Accumulating Molecular Motors

Abstract

Mixtures of filaments and molecular motors form active materials with diverse dynamical behaviors that vary based on their constituents’ molecular properties. To develop a multiscale of these materials, we map the nonequilibrium phase diagram of microtubules and tip-accumulating kinesin-4 molecular motors. We find that kinesin-4 can drive either global contractions or turbulentlike extensile dynamics, depending on the concentrations of both microtubules and a bundling agent. We also observe a range of spatially heterogeneous nonequilibrium phases, including finite-sized radial asters, 1D wormlike chains, extended 2D bilayers, and system-spanning 3D active foams. Finally, we describe intricate kinetic pathways that yield microphase separated structures and arise from the inherent frustration between the orientational order of filamentous microtubules and the positional order of tip-accumulating molecular motors. Our work reveals a range of novel active states. It also shows that the form of active stresses is not solely dictated by the properties of individual motors and filaments, but is also contingent on the constituent concentrations and spatial arrangement of motors on the filaments.

Alternate abstract:

Plain Language Summary

Studies of active matter—collections of energy-consuming animate objects—seek to identify universal patterns that emerge across scales, from collections of animals to nanometer-sized molecular motors. Within this overall effort, one promising direction aims to reconstruct the remarkable properties of living organisms in simplified materials, using well-characterized biochemical building blocks. Motivated by such considerations, we describe a new class of self-organized structures in a mixture of micrometer-long stiff filaments and molecular motors that step along and accumulate at the filament end. The end-bound motors collect the filaments into evolving shapes of varying dimensionalities.

In particular, our work demonstrates the motor-driven hierarchical organization of filaments into radial asters, 2D extended bilayers, and 3D active foamlike materials. Once fully formed, these materials continue to exhibit motor-driven rearrangements. Taken together, our findings demonstrate a new category of nonequilibrium dynamics that we name “active microphase separation.” The dynamics are reminiscent of the equilibrium microphase separation of heterogeneous molecules, which have covalently linked but chemically immiscible segments. In contrast to the equilibrium self-assembly of such heterogeneous molecules, active microphase separation is driven by segmented microtubules whose spatial mesoscale patterns are encoded in the unique dynamical properties of nanosized molecular motors.

Assembly of microphase-separated active materials such as 3D active foams bridges the simplicity of conventional foams and the complexity of biological tissues, exhibiting unique mechanics and self-recycling dynamics. Such discoveries pose fundamental questions in physics while also providing a promising experimental platform for creating mechanically self-regulating soft materials.