Abstract

Cellular interactions are subject to random fluctuations (noise) in quantities of interacting molecules. Noise presents a major challenge for the robust function of natural and engineered cellular networks. Past studies have analyzed how noise is regulated at the intracellular level. Cell–cell communication, however, may provide a complementary strategy to achieve robust gene expression by enabling the coupling of a cell with its environment and other cells. To gain insight into this issue, we have examined noise regulation by quorum sensing (QS), a mechanism by which many bacteria communicate through production and sensing of small diffusible signals. Using a stochastic model, we analyze a minimal QS motif in Gram-negative bacteria. Our analysis shows that diffusion of the QS signal, together with fast turnover of its transcriptional regulator, attenuates low-frequency components of extrinsic noise. We term this unique mechanism “diffusional dissipation” to emphasize the importance of fast signal turnover (or dissipation) by diffusion. We further show that this noise attenuation is a property of a more generic regulatory motif, of which QS is an implementation. Our results suggest that, in a QS system, an unstable transcriptional regulator may be favored for regulating expression of costly proteins that generate public goods.

Highlights

  • Cellular processes are subject to random fluctuations in quantities of interacting molecules

  • quorum sensing (QS) has been shown to control diverse physiological functions in numerous types of bacteria. It provides an elegant strategy for bacteria to sense their density and to achieve coordinated population behavior

  • We show that QS can effectively reduce variability (‘‘noise’’) in the expression of its target genes

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Summary

Introduction

Cellular processes are subject to random fluctuations (or noise) in quantities of interacting molecules. Cells may take advantage of noise to achieve diverse functions [1,2]. In a mechanism called stochastic resonance, noise may improve detection of weak periodic input signals [3], whereas stochastic focusing may turn a gradual response into a threshold-like response [4]. Noise is often exploited to initiate cell differentiation or phenotypic switching. A classical example is the lysis-lysogeny decision in phage l development, where noise is necessary to trigger the decision [5]. Noise is implicated in the competence development of Bacillus subtilis [6]

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