Mechanism of bidirectional thermotaxis in Escherichia coli.

Anja Paulick,Ned S Wingreen,Vladimir Jakovljevic,Victor Sourjik,Yigal Meir,Alex Groisman,William S Ryu,Siming Zhang,Michael Erickstad

doi:10.7554/elife.26607

Abstract

In bacteria various tactic responses are mediated by the same cellular pathway, but sensing of physical stimuli remains poorly understood. Here, we combine an in-vivo analysis of the pathway activity with a microfluidic taxis assay and mathematical modeling to investigate the thermotactic response of Escherichia coli. We show that in the absence of chemical attractants E. coli exhibits a steady thermophilic response, the magnitude of which decreases at higher temperatures. Adaptation of wild-type cells to high levels of chemoattractants sensed by only one of the major chemoreceptors leads to inversion of the thermotactic response at intermediate temperatures and bidirectional cell accumulation in a thermal gradient. A mathematical model can explain this behavior based on the saturation-dependent kinetics of adaptive receptor methylation. Lastly, we find that the preferred accumulation temperature corresponds to optimal growth in the presence of the chemoattractant serine, pointing to a physiological relevance of the observed thermotactic behavior.

Highlights

For many organisms temperature is one of the crucial environmental factors that determine growth and fitness
The time course of subsequent adaptation in the presence of persistent stimulation was similar for thermal and chemical stimuli, indicating that the adaptation to temperature relies on the CheR/CheB receptor methylation system
This was directly confirmed by measuring the methylation profile of Tsr and Tar, both of which shifted towards higher-methylated states at higher temperature (Figure 1—figure supplement 2)

Summary

Introduction

For many organisms temperature is one of the crucial environmental factors that determine growth and fitness. In eukaryotes temperature is usually sensed by specific thermal sensors, behavioral controls by temperature and chemical stimuli are tightly intertwined in the well-studied examples of Caenorhabditis elegans (Kimata et al, 2012) and Drosophila melanogaster (Montell, 2013; Ni et al, 2013). Such integration of behavioral responses is even more pronounced in bacteria. The tactic behavior of E. coli generally relies on the control of flagellar motors by a signaling pathway that decreases the rate of ‘tumbles’ (reorientations) upon an increase in the levels of attractants or upon a decrease in the levels of repellents.

Methods

Results

Conclusion