Title: Stochastic Ratcheting on a Funneled Energy Landscape is Necessary for Highly Efficient Contractility of Actomyosin Force Dipoles,
Abstract: Current understanding of how contractility emerges in disordered actomyosin
networks of non-muscle cells is still largely based on the intuition derived
from earlier works on muscle contractility. This view, however, largely
overlooks the free energy gain following passive cross-linker binding, which,
even in the absence of active fluctuations, provides a thermodynamic drive
towards highly overlapping filamentous states. In this work, we shed light on
this phenomenon, showing that passive cross-linkers, when considered in the
context of two anti-parallel filaments, generate noticeable contractile forces.
However, as binding free energy of cross-linkers is increased, a sharp onset of
kinetic arrest follows, greatly diminishing effectiveness of this contractility
mechanism, allowing the network to contract only with weakly resisting tensions
at its boundary. We have carried out stochastic simulations elucidating this
mechanism, followed by a mean-field treatment that predicts how contractile
forces asymptotically scale at small and large binding energies, respectively.
Furthermore, when considering an active contractile filament pair, based on
non-muscle myosin II, we found that the non-processive nature of these motors
leads to highly inefficient force generation, due to recoil slippage of the
overlap during periods when the motor is dissociated. However, we discovered
that passive cross-linkers can serve as a structural ratchet during these
unbound motor time spans, resulting in vast force amplification. Our results
shed light on the non-equilibrium effects of transiently binding proteins in
biological active matter, as observed in the non-muscle actin cytoskeleton,
showing that highly efficient contractile force dipoles result from synergy of
passive cross-linker and active motor dynamics, via a ratcheting mechanism on a
funneled energy landscape.