Living systems are intrinsically nonequilibrium: They use metabolically derived chemical energy to power their emergent dynamics and self-organization. A crucial driver of these dynamics is the cellular cytoskeleton, a defining example of an active material where the energy injected by molecular motors cascades across length scales, allowing the material to break the constraints of thermodynamic equilibrium and display emergent nonequilibrium dynamics only possible due to the constant influx of energy. Notwithstanding recent experimental advances in the use of local probes to quantify entropy production and the breaking of detailed balance, little is known about the energetics of active materials or how energy propagates from the molecular to emergent length scales. Here, we use a recently developed picowatt calorimeter to experimentally measure the energetics of an active microtubule gel that displays emergent large-scale flows. We find that only approximately one-billionth of the system’s total energy consumption contributes to these emergent flows. We develop a chemical kinetics model that quantitatively captures how the system’s total thermal dissipation varies with ATP and microtubule concentrations but that breaks down at high motor concentration, signaling an interference between motors. Finally, we estimate how energy losses accumulate across scales. Taken together, these results highlight energetic efficiency as a key consideration for the engineering of active materials and are a powerful step toward developing a nonequilibrium thermodynamics of living systems.
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A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers
Understanding the role of nonequilibrium driving in self-organization is crucial for developing a predictive description of biological systems, yet it is impeded by their complexity. The actin cytoskeleton serves as a paradigm for how equilibrium and nonequilibrium forces combine to give rise to self-organization. Motivated by recent experiments that show that actin filament growth rates can tune the morphology of a growing actin bundle cross-linked by two competing types of actin-binding proteins [S. L. Freedman et al. , Proc. Natl. Acad. Sci. U.S.A. 116, 16192–16197 (2019)], we construct a minimal model for such a system and show that the dynamics of a growing actin bundle are subject to a set of thermodynamic constraints that relate its nonequilibrium driving, morphology, and molecular fluxes. The thermodynamic constraints reveal the importance of correlations between these molecular fluxes and offer a route to estimating microscopic driving forces from microscopy experiments.
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- Award ID(s):
- 2011854
- NSF-PAR ID:
- 10313808
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 38
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2102881118
