Importance of Multiple Methylation Sites in Escherichia coli Chemotaxis

PLoS One. 2015 Dec 18;10(12):e0145582. doi: 10.1371/journal.pone.0145582. eCollection 2015.

Abstract

Bacteria navigate within inhomogeneous environments by temporally comparing concentrations of chemoeffectors over the course of a few seconds and biasing their rate of reorientations accordingly, thereby drifting towards more favorable conditions. This navigation requires a short-term memory achieved through the sequential methylations and demethylations of several specific glutamate residues on the chemotaxis receptors, which progressively adjusts the receptors' activity to track the levels of stimulation encountered by the cell with a delay. Such adaptation also tunes the receptors' sensitivity according to the background ligand concentration, enabling the cells to respond to fractional rather than absolute concentration changes, i.e. to perform logarithmic sensing. Despite the adaptation system being principally well understood, the need for a specific number of methylation sites remains relatively unclear. Here we systematically substituted the four glutamate residues of the Tar receptor of Escherichia coli by non-methylated alanine, creating a set of 16 modified receptors with a varying number of available methylation sites and explored the effect of these substitutions on the performance of the chemotaxis system. Alanine substitutions were found to desensitize the receptors, similarly but to a lesser extent than glutamate methylation, and to affect the methylation and demethylation rates of the remaining sites in a site-specific manner. Each substitution reduces the dynamic range of chemotaxis, by one order of magnitude on average. The substitution of up to two sites could be partly compensated by the adaptation system, but the full set of methylation sites was necessary to achieve efficient logarithmic sensing.

Publication types

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

MeSH terms

  • Chemotaxis*
  • DNA Methylation
  • DNA, Bacterial / genetics
  • Escherichia coli / genetics*
  • Escherichia coli / physiology
  • Escherichia coli Proteins / genetics
  • Gene Expression Regulation, Bacterial
  • Receptors, Cell Surface / genetics

Substances

  • DNA, Bacterial
  • Escherichia coli Proteins
  • Receptors, Cell Surface
  • Tar protein, E coli