Universal architecture of bacterial chemoreceptor arrays

  1. Ariane Briegela,b,
  2. Davi R. Ortegac,d,
  3. Elitza I. Tochevaa,
  4. Kristin Wuichetd,
  5. Zhuo Lia,b,
  6. Songye Chena,
  7. Axel Müllere,
  8. Cristina V. Iancua,1,
  9. Gavin E. Murphya,2,
  10. Megan J. Dobroa,
  11. Igor B. Zhulind,f and
  12. Grant J. Jensena,b,3
  1. Divisions of aBiology and
  2. eChemistry and
  3. bHoward Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125;
  4. Departments of cPhysics and
  5. dMicrobiology, University of Tennessee, Knoxville, TN 37996; and
  6. fBioEnergy Center and Computer Science and Mathematics Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831
  • 1Present address: Department of Biochemistry and Molecular Biology, Rosalind Franklin University, The Chicago Medical School, North Chicago, IL 60064.

  • 2Present address: Laboratory of Cell Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892.

  1. Edited by Laura L. Kiessling, University of Wisconsin, Madison, WI, and approved July 20, 2009 (received for review May 11, 2009)

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.

Footnotes

  • 3To whom correspondence should be addressed. E-mail: jensen{at}caltech.edu
  • 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 declare no conflict of interest.

  • This article is a PNAS Direct Submission.