Relationship between cellular response and behavioral variability in bacterial chemotaxis

TL;DR

This study links the architecture of bacterial chemotaxis signaling to observed behavioral variability, showing how stochastic fluctuations and system design influence cellular responses and navigation efficiency.

Contribution

It reveals how the non-linear receptor-kinase system amplifies stochastic fluctuations, affecting behavioral variability and chemotactic response in E. coli.

Findings

Behavioral variability arises from the sigmoidal activation curve.

Fluctuations are amplified by the receptor-kinase architecture.

System tuning balances random spread and gradient response.

Abstract

Bacterial chemotaxis in Escherichia coli is a canonical system for the study of signal transduction. A remarkable feature of this system is the coexistence of precise adaptation in population with large fluctuating cellular behavior in single cells (Korobkova et al. 2004, Nature, 428, 574). Using a stochastic model, we found that the large behavioral variability experimentally observed in non-stimulated cells is a direct consequence of the architecture of this adaptive system. Reversible covalent modification cycles, in which methylation and demethylation reactions antagonistically regulate the activity of receptor-kinase complexes, operate outside the region of first-order kinetics. As a result, the receptor-kinase that governs cellular behavior exhibits a sigmoidal activation curve. This curve simultaneously amplifies the inherent stochastic fluctuations in the system and lengthens the relaxation time in response to stimulus. Because stochastic fluctuations cause large behavioral variability and the relaxation time governs the average duration of runs in response to small stimuli, cells with the greatest fluctuating behavior also display the largest chemotactic response. Finally, Large-scale simulations of digital bacteria suggest that the chemotaxis network is tuned to simultaneously optimize the random spread of cells in absence of nutrients and the cellular response to gradients of attractant.