Optimal Noise Filtering in the Chemotactic Response of Escherichia coli

Abstract

Information-carrying signals in the real world are often obscured by noise. A challenge for any system is to filter the signal from the corrupting noise. This task is particularly acute for the signal transduction network that mediates bacterial chemotaxis, because the signals are subtle, the noise arising from stochastic fluctuations is substantial, and the system is effectively acting as a differentiator which amplifies noise. Here, we investigated the filtering properties of this biological system. Through simulation, we first show that the cutoff frequency has a dramatic effect on the chemotactic efficiency of the cell. Then, using a mathematical model to describe the signal, noise, and system, we formulated and solved an optimal filtering problem to determine the cutoff frequency that bests separates the low-frequency signal from the high-frequency noise. There was good agreement between the theory, simulations, and published experimental data. Finally, we propose that an elegant implementation of the optimal filter in combination with a differentiator can be achieved via an integral control system. This paper furnishes a simple quantitative framework for interpreting many of the key notions about bacterial chemotaxis, and, more generally, it highlights the constraints on biological systems imposed by noise.

Synopsis

Bacterial motility involves successive periods of relatively straight runs, interspersed by tumbles—periods in which the bacteria are reoriented randomly. To move in the direction of chemical gradients—a process known as chemotaxis—cells modulate the duration of the runs. To ascertain whether the direction of the current run is desirable, cells continuously monitor temporal changes in the chemoattractant concentration. However, the decisions can only be based on imperfect information about the environment because binding noise implies that receptor occupancy is a limited measure of the chemoattractant concentration. Bacteria cope by filtering the sensed signal to reduce the effect of this binding noise. Through simulations, Andrews, Yi, and Iglesias demonstrate that there is a particular filter cutoff frequency that achieves optimal chemotaxis. Moreover, using a model of the sensing mechanism, the authors also compute the theoretically optimal system for estimating the chemoattractant concentration from the noisy receptor-occupancy signal. Andrews and colleagues show that these two filtering systems are closely matched, and that their frequency-dependent behavior corresponds to published experimental data. Their results highlight the constraints that noise places on cellular performance as well as demonstrating how cells have evolved to deal with this uncertainty in an optimal fashion.