The Role of Adaptation in Bacterial Speed Races

PLoS Comput Biol. 2016 Jun 3;12(6):e1004974. doi: 10.1371/journal.pcbi.1004974. eCollection 2016 Jun.

Abstract

Evolution of biological sensory systems is driven by the need for efficient responses to environmental stimuli. A paradigm among prokaryotes is the chemotaxis system, which allows bacteria to navigate gradients of chemoattractants by biasing their run-and-tumble motion. A notable feature of chemotaxis is adaptation: after the application of a step stimulus, the bacterial running time relaxes to its pre-stimulus level. The response to the amino acid aspartate is precisely adapted whilst the response to serine is not, in spite of the same pathway processing the signals preferentially sensed by the two receptors Tar and Tsr, respectively. While the chemotaxis pathway in E. coli is well characterized, the role of adaptation, its functional significance and the ecological conditions where chemotaxis is selected, are largely unknown. Here, we investigate the role of adaptation in the climbing of gradients by E. coli. We first present theoretical arguments that highlight the mechanisms that control the efficiency of the chemotactic up-gradient motion. We discuss then the limitations of linear response theory, which motivate our subsequent experimental investigation of E. coli speed races in gradients of aspartate, serine and combinations thereof. By using microfluidic techniques, we engineer controlled gradients and demonstrate that bacterial fronts progress faster in equal-magnitude gradients of serine than aspartate. The effect is observed over an extended range of concentrations and is not due to differences in swimming velocities. We then show that adding a constant background of serine to gradients of aspartate breaks the adaptation to aspartate, which results in a sped-up progression of the fronts and directly illustrate the role of adaptation in chemotactic gradient-climbing.

MeSH terms

  • Adaptation, Physiological / physiology*
  • Aspartic Acid
  • Chemotactic Factors / metabolism
  • Chemotaxis / physiology*
  • Computational Biology
  • Escherichia coli / physiology*
  • Models, Biological*
  • Serine

Substances

  • Chemotactic Factors
  • Aspartic Acid
  • Serine

Grants and funding

This work was supported by the National Science Foundation, Program PoLS, Grant 1411313. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.