Nonequilibrium dissipation in living oocytes

Abstract

-Living organisms are inherently out-of-equilibrium systems. We employ recent developments in stochastic energetics and rely on a minimal microscopic model to predict the amount of mechanical energy dissipated by such dynamics. Our model includes complex rheological effects and nonequilibrium stochastic forces. By performing active microrheology and tracking micronsized vesicles in the cytoplasm of living oocytes, we provide unprecedented measurements of the spectrum of dissipated energy. We show that our model is fully consistent with the experimental data, and we use it to offer predictions for the injection and dissipation energy scales involved in active fluctuations.Perrin's century old picture [1] where the Brownian motion of a colloid results from the many collisions exerted by the solvent's molecules is a cornerstone of soft-matter physics. Langevin [2] modeled the ensuing energy exchanges between the solvent and the colloidal particle in terms of a dissipation channel and energy injection kicks. The key ingredient in the success of that theory was to completely integrate out the "uninteresting" degrees of freedom of the solvent whose properties are gathered in a friction constant and a temperature. In this work we take exactly the reverse stance and ask how, by observing the motion of a tracer embedded in a living medium, one can infer the amount of energy exchange and dissipation with the surrounding medium. The main goal is to quantify the energetic properties of the medium, both injection and dissipation-wise. This is a stimulating question because there are of course striking differences between a living cell and its equilibrium polymer gel counterpart, to which newly developed [3, 4] methods of nonequilibrium statistical mechanics apply. Beyond thermal exchanges that fall within the scope of a Langevin approach, ATP consumption fuels molecular motor activity and drives relentless rearrangement of the cytoskeleton. This chemically driven continuous injection and dissipation of energy adds a nonequilibrium channel that eludes straightforward quantitative analysis. In short, a living cell is not only a fertile playground for testing new ideas from nonequilibrium physics, but also one in which these ideas can lead to a quantitative evaluation of an otherwise ill-understood activity which is of intrinsic biophysical interest. Our work addresses both aspects by a combination of active microrheology, tracking experiments, and theoretical modeling.One experimental way to access nonequilibrium physics in the intracellular medium is to focus on the deviation from thermal equilibrium behavior of the tracer's position statistics: forming the ratio of the response of the tracer's position to an infinitesimal external perturbation to its unperturbed mean-square displacement leads to a quantity that only reduces to the inverse temperature when in p-1 arXiv:1511.00921v2 [q-bio.SC]

Localization and diffusion of tracer particles in viscoelastic media with active force dipoles

“…The present analysis is however done entirely within the original description [10] in order to demonstrate what should be expected in its framework. Remarkably, we could then reproduce the phenomenological model [9] that shows good agreement with the experimental data for eukaryotic cells (see also the related publication [19]). Extensions and generalizations of our results to other models of gels can be performed, and this will be the task of additional work.…”

“…(17), only the force dipoles acting on the fluid component of the medium are affecting the relative velocity w in eq. (19). Equation (17) can be used to obtain an effective equation of motion for the deformation tracer immobilized in the elastic component.…”

Dissipation controls transport and phase transitions in active fluids: mobility, diffusion and biased ensembles

“…The amount of dissipated energy  is defined from purely mechanical arguments as the rate of work that the particles exert on the solvent [47][48][49][50]:…”

Inferring broken detailed balance in the absence of observable currents

“…Often the manifestation of irreversibility is quite dramatic, signalled by di-rected flow or movement, as in transport through mesoscopic devices [6], traveling waves in nonlinear chemical reactions [7], directed motion of molecular motors along biopolymers [8], and the periodic beating of a cell's flagellum [9,10] or cilia [11]. This observation has led to a handful of experimentally-validated methods to identify irreversible behavior by confirming the existence of such flows or fluxes [3,[12][13][14]. However, in the absence of directed motion, it can be challenging to determine if an observed system is out of equilibrium, especially in small noisy systems where fluctuations could mask any obvious irreversibility [15].…”