Thermodynamic Control of Activity Patterns in Cytoskeletal Networks

Abstract

Biological materials, such as the actin cytoskeleton, exhibit remarkable structural adaptability to various external stimuli by consuming different amounts of energy. In this Letter, we use methods from large deviation theory to identify a thermodynamic control principle for structural transitions in a model cytoskeletal network. Specifically, we demonstrate that biasing the dynamics with respect to the work done by nonequilibrium components effectively renormalizes the interaction strength between such components, which can eventually result in a morphological transition. Our work demonstrates how a thermodynamic quantity can be used to renormalize effective interactions, which in turn can tune structure in a predictable manner, suggesting a thermodynamic principle for the control of cytoskeletal structure and dynamics.

Microscopic interactions control a structural transition in active mixtures of microtubules and molecular motors

“…Such extensile flows have been reported for both microtubule/kinesin [14] and actomyosin [29,30] based materials. Theoretical work has suggested that extensile stresses could arise from the polarity sorting of filaments [31] or the mechanical properties of the motors themselves [32,33]. Under other conditions, both microtubule and actin-based active gels have been found to undergo bulk contraction.…”

Methods and conversations in (post)modern thermodynamics

“…Similar DPTs have been described through the application of LDT to the distribution of entropy production in systems such as active Brownian particles, with a phase transition marked by a collective particle alignment [86]. Furthermore, LDT may aid in uncovering DPTs in other systems, such as chemical reaction networks or conformational changes in energy-driven biomolecules, by identifying rare dynamical regimes of their dynamics [225]. At larger scales, in the area of climatology and geophysical modeling, LDT has gained prominence in evaluating climate anomalies, including sustained, long-term heat waves across spatially extended regions (see Fig.…”

Self-organization in amoeboid motility

“…Yet, these models pre-suppose a particular migration mechanism, and the mechanism for upstream choice of which mode to choose from is left open. Though far removed from the complexity of a whole cell, some inspiration might come from thermodynamic control theory applied to networks of out-of-equilibrium filaments, such as the cytoskeleton Lamtyugina et al (2021). Based on this work, it has been suggested that energy resources and external cues could effectively modify cytoskeletal material properties and drive transitions between many-filament structures Lamtyugina et al (2021).…”

“…Though far removed from the complexity of a whole cell, some inspiration might come from thermodynamic control theory applied to networks of out-of-equilibrium filaments, such as the cytoskeleton Lamtyugina et al (2021). Based on this work, it has been suggested that energy resources and external cues could effectively modify cytoskeletal material properties and drive transitions between many-filament structures Lamtyugina et al (2021). It will be interesting to apply this approach to active droplets in which different migration modes can be associated with dynamic structural transitions of the material.…”