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Open Access Highly Accessed Research article

Effects of receptor modification and temperature on dynamics of sensory complexes in Escherichia coli chemotaxis

Sonja Schulmeister12, Karin Grosse1 and Victor Sourjik1*

Author Affiliations

1 Zentrum für Molekulare Biologie der Universität Heidelberg, DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany

2 BioQuant, Im Neuenheimer Feld 267, 69120 Heidelberg, Germany

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BMC Microbiology 2011, 11:222  doi:10.1186/1471-2180-11-222

Published: 6 October 2011

Abstract

Background

Extracellular stimuli in chemotaxis of Escherichia coli and other bacteria are processed by large clusters of sensory complexes. The stable core of these clusters is formed by transmembrane receptors, a kinase CheA, and an adaptor CheW, whereas adaptation enzymes CheR and CheB dynamically associate with the clusters via interactions with receptors and/or CheA. Several biochemical studies have indicated the dependence of the sensory complex stability on the adaptive modification state of receptors and/or on temperature, which may potentially allow environment-dependent tuning of its signalling properties. However, the extent of such regulation in vivo and its significance for chemotaxis remained unclear.

Results

Here we used fluorescence recovery after photobleaching (FRAP) to confirm in vivo that the exchange of CheA and CheW shows a modest dependency on the level of receptor modification/activity. An even more dramatic effect was observed for the exchange kinetics of CheR and CheB, indicating that their association with clusters may depend on the ability to bind substrate sites on receptors and on the regulatory phosphorylation of CheB. In contrast, environmental temperature did not have a discernible effect on stability of the cluster core. Strain-specific loss of E. coli chemotaxis at high temperature could instead be explained by a heat-induced reduction in the chemotaxis protein levels. Nevertheless, high basal levels of chemotaxis and flagellar proteins in common wild type strains MG1655 and W3110 enabled these strains to maintain their chemotactic ability up to 42°C.

Conclusions

Our results confirmed that clusters formed by less modified receptors are more dynamic, which can explain the previously observed adjustment of the chemotaxis response sensitivity according to the level of background stimulation. We further propose that the dependency of CheR exchange on the availability of unmethylated sites on receptors is important to improve the overall chemotaxis efficiency by suppressing molecular noise under conditions of high ligand concentrations. Moreover, the observed stability of the cluster core at high temperature is in line with the overall thermal robustness of the chemotaxis pathway and allows maintenance of chemotaxis up to 42°C in the common wild type strains of E. coli.