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Broken detailed balance at mesoscopic scales in active biological systems

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Science  29 Apr 2016:
Vol. 352, Issue 6285, pp. 604-607
DOI: 10.1126/science.aac8167

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Identifying nonequilibrium dynamics

Living systems clearly operate out of thermodynamic equilibrium at the molecular scale. How these activities are manifest at the cellular scale, however, has been unclear. Battle et al. use video microscopy together with statistical thermodynamics to unambiguously identify which random fluctuations at the cellular scale are out of equilibrium (see the Perspective by Rupprecht and Prost). Transitions between states obey a detailed balance in equilibrium, whereas imbalanced transitions point to nonequilibrium dynamics. For instance, nonequilibrium dynamics can be identified in the periodic beating of a flagellum and in the nonperiodic fluctuations of primary cilia.

Science, this issue p. 604; see also p. 514

Abstract

Systems in thermodynamic equilibrium are not only characterized by time-independent macroscopic properties, but also satisfy the principle of detailed balance in the transitions between microscopic configurations. Living systems function out of equilibrium and are characterized by directed fluxes through chemical states, which violate detailed balance at the molecular scale. Here we introduce a method to probe for broken detailed balance and demonstrate how such nonequilibrium dynamics are manifest at the mesosopic scale. The periodic beating of an isolated flagellum from Chlamydomonas reinhardtii exhibits probability flux in the phase space of shapes. With a model, we show how the breaking of detailed balance can also be quantified in stationary, nonequilibrium stochastic systems in the absence of periodic motion. We further demonstrate such broken detailed balance in the nonperiodic fluctuations of primary cilia of epithelial cells. Our analysis provides a general tool to identify nonequilibrium dynamics in cells and tissues.

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