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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.
https://doi.org/10.7554/eLife.26607.001Many bacteria can move towards or away from chemicals, heat and other stimuli in their environment. The ability of bacteria to move in response to nutrients and other chemicals, known as chemotaxis, is the best understood of these phenomena. Bacteria generally swim in a fairly random way and frequently change direction. During chemotaxis, however, the bacteria sense changes in the concentrations of a chemical in their surroundings and this biases the direction in which they swim so that they spend more time swimming towards or away from the source of the chemical. The bacteria have various receptor proteins that can detect different chemicals. For example, the Tar and Tsr receptors can recognize chemicals called aspartate and serine, respectively, which are – amongst other things – nutrients that are used to build proteins.
Tar and Tsr are also involved in the response to temperature, referred to as thermotaxis. At low temperatures, a bacterium Escherichia coli will move towards sources of heat. Yet when the bacteria detect both serine and aspartate they may reverse the response and move towards colder areas instead. However, it was not clear why the bacteria do this, and what roles Tar and Tsr play in this response.
Paulick et al. have now combined approaches that directly visualise signalling inside living bacteria and that track the movements of individual bacterial cellswith mathematical modelling to investigate thermotaxis in E. coli. The experiments show that the bacteria’s behaviour could be explained by interplay between the responses mediated by Tar and Tsr. In the absence of both serine and aspartate, both receptors stimulate heat-seeking responses, causing the bacteria to move towards hotter areas. When only aspartate is present, Tsr continues to stimulate the heat-seeking response, but the aspartate causes Tar to switch to promoting a cold-seeking response instead. This leads to the bacteria accumulating in areas of intermediate temperature. In the presence of serine only, the bacteria behave in a similar way because the receptors swap roles so that Tsr stimulates the cold-seeking response, while Tar promotes the heat-seeking one.
The intermediate temperature at which the bacteria accumulate in response to serine is also around the optimal temperature for E.coli growth in presence of this chemical, suggesting that thermotaxis might play an important role in allowing bacteria to survive and grow in many different environments, including in the human body. Thus, understanding how chemotaxis and thermotaxis are regulated may lead to new ways to control how bacteria behave in patients and natural environments.
https://doi.org/10.7554/eLife.26607.002