Functional interactions between receptors in bacterial chemotaxis

Abstract

Bacterial chemotaxis is a model system for signal transduction, noted for its relative simplicity, high sensitivity, wide dynamic range and robustness. Changes in ligand concentrations are sensed by a protein assembly consisting of transmembrane receptors, a coupling protein (CheW) and a histidine kinase (CheA)1,2,3,4. In Escherichia coli, these components are organized at the cell poles in tight clusters that contain several thousand copies of each protein1,4,5,6. Here we studied the effects of variation in the composition of clusters on the activity of the kinase and its sensitivity to attractant stimuli, monitoring responses in vivo using fluorescence resonance energy transfer. Our results indicate that assemblies of bacterial chemoreceptors work in a highly cooperative manner, mimicking the behaviour of allosteric proteins. Conditions that favour steep responses to attractants in mutants with homogeneous receptor populations also enhance the sensitivity of the response in wild-type cells. This is consistent with a number of models7,8,9,10,11 that assume long-range cooperative interactions between receptors as a general mechanism for signal integration and amplification.

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Figure 1: Effect of the homogeneity of the receptor cluster on response to attractants.
Figure 2: Effect of the composition of the receptor–kinase complex on response to attractants.
Figure 3: Cross-talk between receptors in different modification states and between different types of receptor.
Figure 4: Effect of complex stoichiometry on response of CheR+ CheB+ cells to attractant.

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Acknowledgements

We thank J. S. Parkinson for providing some of the plasmids, strains and antibody used in this study, and R. C. Stewart for providing antibody. We also thank D. Bray, K. A. Fahrner, J. J. Falke, J. S. Parkinson, T. Shimizu and A. Vaknin for comments on the manuscript. We thank P. Zucchi for technical help. This research was supported by the NIH.

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Correspondence to Howard C. Berg.

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Supplementary information

Supplementary information 1

Data analysis and simulations. (DOC 39 kb)

Supplementary information 2

Strains. (DOC 27 kb)

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Sourjik, V., Berg, H. Functional interactions between receptors in bacterial chemotaxis. Nature 428, 437–441 (2004). https://doi.org/10.1038/nature02406

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