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

Silke Neumann, Clinton H. Hansen, Ned S. Wingreen, Victor Sourjik

Research output: Contribution to journalArticle

49 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)3484-3495
Number of pages12
JournalEMBO Journal
Volume29
Issue number20
DOIs
StatePublished - Oct 2010

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Keywords

  • FRET
  • bacterial chemotaxis
  • signal integration
  • signal transduction
  • transport

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