Published October 6, 2009 | Version Published + Supplemental Material
Journal Article Open

Universal architecture of bacterial chemoreceptor arrays

Abstract

Chemoreceptors are key components of the high-performance signal transduction system that controls bacterial chemotaxis. Chemoreceptors are typically localized in a cluster at the cell pole, where interactions among the receptors in the cluster are thought to contribute to the high sensitivity, wide dynamic range, and precise adaptation of the signaling system. Previous structural and genomic studies have produced conflicting models, however, for the arrangement of the chemoreceptors in the clusters. Using whole-cell electron cryo-tomography, here we show that chemoreceptors of different classes and in many different species representing several major bacterial phyla are all arranged into a highly conserved, 12-nm hexagonal array consistent with the proposed "trimer of dimers" organization. The various observed lengths of the receptors confirm current models for the methylation, flexible bundle, signaling, and linker sub-domains in vivo. Our results suggest that the basic mechanism and function of receptor clustering is universal among bacterial species and was thus conserved during evolution.

Additional Information

© 2009 National Academy of Sciences. Edited by Laura L. Kiessling, University of Wisconsin, Madison, WI, and approved July 20, 2009 (received for review May 11, 2009). Author contributions: A.B. and G.J.J. designed research; A.B., D.R.O., E.I.T., K.W., Z.L., S.C., A.M., C.V.I., G.E.M., and M.J.D. performed research; A.B., D.R.O., E.I.T., K.W., and I.B.Z. analyzed data; and A.B., D.R.O., E.I.T., I.B.Z., and G.J.J. wrote the paper. The authors wish to thank Eric Matson, Reinhard Rachel, Kevin Bruhn, Gordon Cannon, Alan Barbour, Sarkis Mazmanian, Jeanette Beatty, Maria Sandkvist, Dianne Newman, and John S. Parkinson for bacterial strains; Howard Berg for the penicillin treatment protocol for E. coli; Jane H. Ding for computational support; Juergen Plitzko, Alasdair McDowall and Jian Shi for EM support; and Roger Alexander, Luke Ulrich, and Bhanu Rekapalli for assistance and helpful suggestions. The authors also thank Professor Wolfgang Baumeister (Max Planck Institute for Biochemistry, Martinsried, Germany) for the permission to include the data from T. maritima (which was collected in his laboratory and under his supervision) in this study. This work was supported in part by National Institutes of Health Grants R01 AI067548 and P50 GM082545 (to G.J.J.) and R01 GM72285 (to I.B.Z.), as well as the Howard Hughes Medical Institute, the Beckman Institute at Caltech, and gifts to Caltech from the Gordon and Betty Moore Foundation and Agouron Institute.

Attached Files

Published - Briegel2009p6071P_Natl_Acad_Sci_Usa.pdf

Supplemental Material - 0905181106SI.pdf

Supplemental Material - Appendix_PDF.pdf

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Additional details

Identifiers

PMCID
PMC2761316
Eprint ID
16387
Resolver ID
CaltechAUTHORS:20091019-151620276

Funding

NIH
R01 AI067548
NIH
P50 GM082545
NIH
R01 GM72285
Howard Hughes Medical Institute (HHMI)
Caltech Beckman Institute
Gordon and Betty Moore Foundation
Agouron Institute

Dates

Created
2009-10-20
Created from EPrint's datestamp field
Updated
2021-11-08
Created from EPrint's last_modified field