Universal energy-accuracy tradeoffs in nonequilibrium cellular sensing

We combine stochastic thermodynamics, large deviation theory, and information theory to derive fundamental limits on the accuracy with which single cell receptors can estimate external concentrations. As expected, if the estimation is performed by an ideal observer of the entire trajectory of receptor states, then no energy consuming nonequilibrium receptor that can be divided into bound and unbound states can outperform an equilibrium two -state receptor. However, when the estimation is performed by a simple observer that measures the fraction of time the receptor is bound, we derive a fundamental limit on the accuracy of general nonequilibrium receptors as a function of energy consumption. We further derive and exploit explicit formulas to numerically estimate a Pareto-optimal tradeoff between accuracy and energy. We find this tradeoff can be achieved by nonuniform ring receptors with a number of states that necessarily increases with energy. Our results yield a thermodynamic uncertainty relation for the time a physical system spends in a pool of states and generalize the classic Berg -Purcell limit [H. C. Berg and E. M. Purcell, Biophys. J. 20, 193 (1977)] on cellular sensing along multiple dimensions.

Automated summary

We use stochastic thermodynamics, large deviation theory, and information theory to establish fundamental limits on the accuracy of single cell receptors in estimating external concentrations. While an ideal observer of receptor states cannot be outperformed by any nonequilibrium receptor, we find that a simple observer measuring the fraction of time the receptor is bound has a fundamental limit on the accuracy of non-equilibrium receptors. We also derive explicit formulas to numerically estimate the tradeoff between accuracy and energy consumption in nonequilibrium receptors.