Filament flexibility enhances power transduction of F-actin bundles

The dynamic behavior of bundles of actin filaments growing against a loaded obstacle is investigated through a generalized version of the standard multifilament Brownian Ratchet model in which the (de)polymerizing filaments are treated not as rigid rods but as semiflexible discrete wormlike chains with a realistic value of the persistence length. By stochastic dynamic simulations, we study the relaxation of a bundle of N_f filaments with a staggered seed arrangement against a harmonic trap load in supercritical conditions. Thanks to the time scale separation between the wall motion and the filament size relaxation, mimicking realistic conditions, this setup allows us to extract a full load-velocity curve from a single experiment over the trap force/size range explored. We observe a systematic evolution of steady nonequilibrium states over three regimes of bundle lengths L. A first threshold length Λ marks the transition between the rigid dynamic regime (L < Λ), characterized by the usual rigid filament load-velocity relationship V(F), and the flexible dynamic regime (L > Λ), where the velocity V(F, L) is an increasing function of the bundle length L at a fixed load F, the enhancement being the result of an improved level of work sharing among the filaments induced by flexibility. A second critical length corresponds to the beginning of an unstable regime characterized by a high probability to develop escaping filaments which start growing laterally and thus do not participate anymore in the generation of the polymerization force. This phenomenon prevents the bundle from reaching at this critical length the limit behavior corresponding to perfect load sharing.