TY - JOUR

T1 - Thermodynamically consistent treatment of the growth of a biopolymer in the presence of a smooth obstacle interaction potential

AU - Motahari, F.

AU - Carlsson, A. E.

N1 - Funding Information:
This work was supported by the National Institute of General Medical Sciences under Grant No. R01 GM107667 and the National Science Foundation under Grant No. CMMI:15-458571.
Funding Information:
This work was supported by the National Institute of General Medical Sciences under Grant No. R01 GM107667 and the National Science Foundation under Grant No. CMMI:15-458571.
Publisher Copyright:
© 2019 American Physical Society.

PY - 2019/10/17

Y1 - 2019/10/17

N2 - We investigate the effect of filament-obstacle interactions on the force-velocity relation of growing biopolymers, via calculations explicitly treating obstacle diffusion and stochastic addition and subtraction of subunits. We first show that the instantaneous subunit on- and off-rates satisfy a rigorous thermodynamic relationship determined by the filament-obstacle interaction potential, which has been violated by several calculations in the literature. The instantaneous rates depend not only on the average force on the obstacle but also on the shape of the potential on the nanometer length scale. Basing obstacle-induced reduction of the on-rate entirely on the force, as previous work has often done, is thermodynamically inconsistent and can overestimate the stall force, sometimes by more than a factor of two. We perform simulations and analytic calculations of the force-velocity relation satisfying the thermodynamic relationship. The force-velocity relation can deviate strongly from the Brownian-Ratchet predictions. For shallow potential wells of depth ∼5kBT, which might correspond to transient filament-membrane attachments, the velocity drops more rapidly than predicted by the Brownian-Ratchet model, in some cases by as much as a factor of 50 at an opposing force of only 1 pN. On the other hand, the zero-force velocity is much less affected than would be expected from naive use of the Boltzmann factor. Furthermore, the growth velocity has a surprisingly strong dependence on the obstacle diffusion coefficient even when the dimensionless diffusion coefficient is large. For deep potential wells, as might result from strong filament-membrane links, both the on- and off-rates are reduced significantly, slowing polymerization. Such potentials can sustain pulling forces while polymerizing but only if the attractive well is relatively flat over a region comparable to or greater than the monomer size. For double-well potentials, which have such a flat region, the slowing of polymerization by external pushing force is almost linear up to the stall force in some parameter ranges.

AB - We investigate the effect of filament-obstacle interactions on the force-velocity relation of growing biopolymers, via calculations explicitly treating obstacle diffusion and stochastic addition and subtraction of subunits. We first show that the instantaneous subunit on- and off-rates satisfy a rigorous thermodynamic relationship determined by the filament-obstacle interaction potential, which has been violated by several calculations in the literature. The instantaneous rates depend not only on the average force on the obstacle but also on the shape of the potential on the nanometer length scale. Basing obstacle-induced reduction of the on-rate entirely on the force, as previous work has often done, is thermodynamically inconsistent and can overestimate the stall force, sometimes by more than a factor of two. We perform simulations and analytic calculations of the force-velocity relation satisfying the thermodynamic relationship. The force-velocity relation can deviate strongly from the Brownian-Ratchet predictions. For shallow potential wells of depth ∼5kBT, which might correspond to transient filament-membrane attachments, the velocity drops more rapidly than predicted by the Brownian-Ratchet model, in some cases by as much as a factor of 50 at an opposing force of only 1 pN. On the other hand, the zero-force velocity is much less affected than would be expected from naive use of the Boltzmann factor. Furthermore, the growth velocity has a surprisingly strong dependence on the obstacle diffusion coefficient even when the dimensionless diffusion coefficient is large. For deep potential wells, as might result from strong filament-membrane links, both the on- and off-rates are reduced significantly, slowing polymerization. Such potentials can sustain pulling forces while polymerizing but only if the attractive well is relatively flat over a region comparable to or greater than the monomer size. For double-well potentials, which have such a flat region, the slowing of polymerization by external pushing force is almost linear up to the stall force in some parameter ranges.

UR - http://www.scopus.com/inward/record.url?scp=85073810596&partnerID=8YFLogxK

U2 - 10.1103/PhysRevE.100.042409

DO - 10.1103/PhysRevE.100.042409

M3 - Article

C2 - 31770877

AN - SCOPUS:85073810596

SN - 2470-0045

VL - 100

JO - Physical Review E - Statistical, Nonlinear, and Soft Matter Physics

JF - Physical Review E - Statistical, Nonlinear, and Soft Matter Physics

IS - 4

M1 - 042409

ER -