Mechanism of bidirectional thermotaxis in Escherichia coli

Elife. 2017 Aug 3:6:e26607. 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.

Keywords: E. coli; bacterial motility; chemotaxis; computational biology; environmental sensing; infectious disease; microbiology; signal transduction; systems biology; temperature; thermotaxis.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological
  • Aspartic Acid / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Chemotactic Factors / pharmacology*
  • Escherichia coli K12 / drug effects*
  • Escherichia coli K12 / genetics
  • Escherichia coli K12 / growth & development
  • Escherichia coli K12 / metabolism
  • Escherichia coli Proteins / genetics*
  • Escherichia coli Proteins / metabolism
  • Fluorescence Resonance Energy Transfer
  • Gene Expression Regulation, Bacterial*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Methyl-Accepting Chemotaxis Proteins / genetics*
  • Methyl-Accepting Chemotaxis Proteins / metabolism
  • Microfluidic Analytical Techniques
  • Receptors, Cell Surface / genetics*
  • Receptors, Cell Surface / metabolism
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Serine / pharmacology
  • Signal Transduction
  • Taxis Response / physiology*
  • Temperature

Substances

  • Bacterial Proteins
  • Chemotactic Factors
  • Cyan Fluorescent Protein
  • Escherichia coli Proteins
  • Luminescent Proteins
  • Methyl-Accepting Chemotaxis Proteins
  • Receptors, Cell Surface
  • Recombinant Fusion Proteins
  • Tar protein, E coli
  • cheY protein, E coli
  • cheZ protein, E coli
  • tsr protein, E coli
  • yellow fluorescent protein, Bacteria
  • Green Fluorescent Proteins
  • Aspartic Acid
  • Serine