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 chaotic flows, locally contractile asters, and bulk contraction. However, it is unclear which protein-scale interactions, if any, set the contractile or extensile nature of the active gel, or how to control the transition from one phase to another in a simple active system. Here, we explore the microscopic origin of the extensile-to-contractile transition in a reconstituted active material composed of stabilized microtubules, depletant, ATP, and clusters of kinesin-1 motors. We show that microscopic interactions between highly processive motor clusters and microtubules can trigger the end-accumulation of motor proteins, which in turn drives polarity sorting and aster formation. Combining experiments and simple scaling arguments, we demonstrate that the extensile-to-contractile transition is akin to a self-assembly process where nematic and polar aligning interactions compete. We identify a single control parameter given by the ratio of the different component concentrations that dictates the material-scale organization into either a contractile aster or an extensile bundle. Overall, this work shows that robust self-organization of cytoskeletal active materials can be controlled by precise biochemical and mechanical tuning at the microscopic level.

Contractile to extensile transitions and mechanical adaptability enabled by activity in cytoskeletal structures

“…This is consistent with contractile to extensile transition observed in the microtubule-kinesin system with increasing ATP (chemical fuel for motor walking) [33, 34]. While competition between nematic alignment and polar sorting has been proposed as a controlling mechanism for this transition [33], our results indicate force-dependent architectural changes can also trigger this transition without any explicit way of affecting nematic alignment (as no volume exclusion between filaments is considered in our system). We see this during bundle elongation (without any changes in overall morphology) in response to applied force.…”

“…The active stress is also different (contractile) in bundles formed due to applied force in contrast to the bundles formed due to changing motor stiffness (extensile). Extensile to contractile transition in active stress has been recently found in experiments with actin-myosin systems [31] and with microtubule-kinesin systems [32][33][34] and the physical mechanism behind this transition is not well understood. In our case, we find contractile to extensile transition in active stress (associated with a morphological transition from aster to bundle) with increasing motor walking speed (Fig.…”