The Role of Adaptation in Bacterial Speed Races.

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 chemotax...

Full description

Bibliographic Details
Main Authors: Jérôme Wong-Ng, Anna Melbinger, Antonio Celani, Massimo Vergassola
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-06-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4892596?pdf=render
id doaj-ac8e784b8307454fbb6e9e41ea65ff71
record_format Article
spelling doaj-ac8e784b8307454fbb6e9e41ea65ff712020-11-25T01:57:43ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582016-06-01126e100497410.1371/journal.pcbi.1004974The Role of Adaptation in Bacterial Speed Races.Jérôme Wong-NgAnna MelbingerAntonio CelaniMassimo VergassolaEvolution 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.http://europepmc.org/articles/PMC4892596?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Jérôme Wong-Ng
Anna Melbinger
Antonio Celani
Massimo Vergassola
spellingShingle Jérôme Wong-Ng
Anna Melbinger
Antonio Celani
Massimo Vergassola
The Role of Adaptation in Bacterial Speed Races.
PLoS Computational Biology
author_facet Jérôme Wong-Ng
Anna Melbinger
Antonio Celani
Massimo Vergassola
author_sort Jérôme Wong-Ng
title The Role of Adaptation in Bacterial Speed Races.
title_short The Role of Adaptation in Bacterial Speed Races.
title_full The Role of Adaptation in Bacterial Speed Races.
title_fullStr The Role of Adaptation in Bacterial Speed Races.
title_full_unstemmed The Role of Adaptation in Bacterial Speed Races.
title_sort role of adaptation in bacterial speed races.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2016-06-01
description 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.
url http://europepmc.org/articles/PMC4892596?pdf=render
work_keys_str_mv AT jeromewongng theroleofadaptationinbacterialspeedraces
AT annamelbinger theroleofadaptationinbacterialspeedraces
AT antoniocelani theroleofadaptationinbacterialspeedraces
AT massimovergassola theroleofadaptationinbacterialspeedraces
AT jeromewongng roleofadaptationinbacterialspeedraces
AT annamelbinger roleofadaptationinbacterialspeedraces
AT antoniocelani roleofadaptationinbacterialspeedraces
AT massimovergassola roleofadaptationinbacterialspeedraces
_version_ 1724972910576140288