Active nematic order and dynamic lane formation of microtubules driven by membrane-bound diffusing motors

Dynamic lane formation and long-range active nematic alignment is reported
using a geometry in which kinesin motors are directly coupled to a lipid
bilayer, allowing for in-plane motor diffusion during microtubule gliding.
We use fluorescence microscopy to image protein distributions in and below
the dense two-dimensional microtubule layer, revealing evidence of
diffusion-enabled kinesin restructuring within the fluid membrane
substrate as microtubules collectively glide above. We find that the lipid
membrane acts to promote filament-filament alignment within the gliding
layer, enhancing the formation of a globally aligned active nematic state.
We also report the emergence of an intermediate, locally ordered state in
which apolar dynamic lanes of nematically-aligned microtubules migrate
across the substrate. To understand this emergent behavior, we implement a
continuum model obtained from coarse graining a collection of
self-propelled rods, with propulsion set by the local motor kinetics.
Tuning the microtubule and kinesin concentrations as well as active
propulsion in these simulations reveals that increasing motor activity
promotes dynamic nematic lane formation. Simulations and experiments show
that, following fluid bilayer substrate mediated spatial motor
restructuring, the total motor concentration becomes enriched below the
microtubule lanes that they drive, with the feedback leading to more
dynamic lanes. Our results have implications for membrane coupled active
nematics in vivo as well as for engineering dynamic and reconfigurable
materials where the structural elements and power sources can dynamically
co-localize, enabling efficient mechanical work.