Microscopic interactions control a structural transition in active mixtures of microtubules and molecular motors

Abstract Microtubules and molecular motors are essential components of the cellular cytoskeleton, driving fundamental processes in vivo, including chromosome segregation and cargo transport. When reconstituted in vitro , these cytoskeletal proteins serve as energy-consuming building blocks to study the self-organization of active matter. Cytoskeletal active gels display rich emergent dynamics, including extensile flows, locally contractile asters, and bulk contraction. However, how the protein-protein interaction kinetics set their contractile or extensile nature is unclear. Here, we explore the origin of the transition from extensile bundles to contractile asters in a minimal reconstituted system composed of stabilized microtubules, depletant, ATP, and clusters of kinesin-1 motors. We show that the microtubule binding and unbinding kinetics of highly processive motor clusters set their ability to end-accumulate, which can drive polarity sorting of the microtubules and aster formation. We further demonstrate that the microscopic time scale of end-accumulation sets the emergent time scale of aster formation. Finally, we show that biochemical regulation is insufficient to explain fully the transition as generic aligning interactions through depletion, crosslinking, or excluded volume interactions can drive bundle formation, despite the presence of end-accumulating motors. The extensile-to-contractile transition is well captured by a simple self-assembly model where nematic and polar aligning interactions compete to form either bundles or asters. Starting from a five-dimensional organization phase space, we identify a single control parameter given by the ratio of the different component concentrations that dictates the material-scale organization. Overall, this work shows that the interplay of biochemical and mechanical tuning at the microscopic level controls the robust self-organization of active cytoskeletal materials. Significance statement Self-organization in living cells is often driven by energy-consuming motor proteins that push and pull on a network of cytoskeletal filaments. However, it is unclear how to connect the emergent structure and dynamics of reconstituted cytoskeletal materials to the kinetics and mechanics of their microscopic building blocks. Here, we systematically correlate bulk structure with asymmetry of the motor distribution along single filaments to explain the transition from extensile bundles to contractile asters in active networks of stabilized microtubules crosslinked by motor proteins. We combine experiments and scaling arguments to identify a single number that predicts how the system will self-organize. This work shows that biochemical and mechanical interactions compete to set the emergent structure of active biomimetic gels.