Differences in signalling by directly and indirectly binding ligands in bacterial chemotaxis

EMBO J. 2010 Oct 20;29(20):3484-95. doi: 10.1038/emboj.2010.224. Epub 2010 Sep 10.

Abstract

In chemotaxis of Escherichia coli and other bacteria, extracellular stimuli are perceived by transmembrane receptors that bind their ligands either directly, or indirectly through periplasmic-binding proteins (BPs). As BPs are also involved in ligand uptake, they provide a link between chemotaxis and nutrient utilization by cells. However, signalling by indirectly binding ligands remains much less understood than signalling by directly binding ligands. Here, we compared intracellular responses mediated by both types of ligands and developed a new mathematical model for signalling by indirectly binding ligands. We show that indirect binding allows cells to better control sensitivity to specific ligands in response to their nutrient environment and to coordinate chemotaxis with ligand transport, but at the cost of the dynamic range being much narrower than for directly binding ligands. We further demonstrate that signal integration by the chemosensory complexes does not depend on the type of ligand. Overall, our data suggest that the distinction between signalling by directly and indirectly binding ligands is more physiologically important than the traditional distinction between high- and low-abundance receptors.

Publication types

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

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Chemotactic Factors / pharmacology
  • Chemotaxis / drug effects
  • Chemotaxis / physiology*
  • Dose-Response Relationship, Drug
  • Escherichia coli / drug effects
  • Escherichia coli / physiology*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Humans
  • Ligands*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Methyl-Accepting Chemotaxis Proteins
  • Models, Theoretical
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*

Substances

  • Bacterial Proteins
  • Chemotactic Factors
  • Escherichia coli Proteins
  • Ligands
  • Membrane Proteins
  • Methyl-Accepting Chemotaxis Proteins