Microtubules as Maxwell's demons: active transport-based phase-separation of a binary motor mixture

by Alfredo Sciortino (CEA Grenoble/ESPCI Paris)

Monday 10 Jun 2024, 12:00 → 13:00 Europe/Rome

Aula Rasetti (Dip. di Fisica - Edificio G. Marconi)

Living cells need to deliver specific cargoes at specific locations. In order to do that, they mostly use molecular motors, a set of proteins able to walk on “cytoskeletal highways”, a highly organized network of polar filaments (microtubules). Since different motors walk in different directions along the filament polarity and since the microtubule network is organized in a radial way, this allows selective transport towards the center or the periphery of the cell. How, however, such a network is formed in the first place remains unknown. Recently, a large number of works have focused on gliding assays (in which immobilized motors propel filaments) and/or on motors/microtubules mixtures (in which freely diffusing motors walk on the filaments) in an attempt to reconstitute cytoskeletal polarity with simple ingredients. Here we show how a minimal system comprising microtubules and of two different kinds of molecular motors, a plus- and a minus-end directed one, can self-organize in polarity-sorted domains.  Molecular motors are bound to a lipid membrane and are hence able to both walk on microtubules and to exert forces, hence displacing them. The final result is that starting from a homogeneous initial distribution of motors and filaments, the system self-organizes into stable domains enriched of motors, separated by an interface of polarity-sorted microtubules. Patterns are formed by local motor fluxes and are maintained by a balance between constant active transport, diffusion of free motors and by the opposite forces the two motors exert along microtubules. In other words, in this minimal system polarity emerges from a self-organization process. We then show how in this system the emergence of polarity sorted domains resembles classical phase separation of binary mixtures. Based on this latter analogy, we also build a continuous model,  treating microtubules as "active pump" or as biological analogues of the classical "Maxwell demon", and show in general terms how phase separation and polarity sorting can be achieved using activity in the form of selective transport of material and discuss this implication both in cellular biology and in physics.