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Research Article

Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins

Ariane Briegel, Xiaoxiao Li, Alexandrine M. Bilwes, Kelly T. Hughes, Grant J. Jensen, and Brian R. Crane
  1. aDivision of Biology, California Institute of Technology, Pasadena, CA 91125;
  2. bDepartment of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853;
  3. cDepartment of Biology, University of Utah, Salt Lake City, UT 84112; and
  4. dHoward Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125

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PNAS March 6, 2012 109 (10) 3766-3771; https://doi.org/10.1073/pnas.1115719109
Ariane Briegel
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Xiaoxiao Li
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Alexandrine M. Bilwes
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Kelly T. Hughes
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Grant J. Jensen
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  • For correspondence: Jensen@caltech.edu bc69@cornell.edu
Brian R. Crane
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  • For correspondence: Jensen@caltech.edu bc69@cornell.edu
  1. Edited by Laura L. Kiessling, University of Wisconsin, Madison, WI, and approved January 13, 2012 (received for review September 23, 2011)

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Abstract

Chemoreceptor arrays are supramolecular transmembrane machines of unknown structure that allow bacteria to sense their surroundings and respond by chemotaxis. We have combined X-ray crystallography of purified proteins with electron cryotomography of native arrays inside cells to reveal the arrangement of the component transmembrane receptors, histidine kinases (CheA) and CheW coupling proteins. Trimers of receptor dimers lie at the vertices of a hexagonal lattice in a “two-facing-two” configuration surrounding a ring of alternating CheA regulatory domains (P5) and CheW couplers. Whereas the CheA kinase domains (P4) project downward below the ring, the CheA dimerization domains (P3) link neighboring rings to form an extended, stable array. This highly interconnected protein architecture underlies the remarkable sensitivity and cooperative nature of transmembrane signaling in bacterial chemotaxis.

  • protein structure
  • hybrid methods
  • two-component systems

Footnotes

  • ↵1A.B. and X.L. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. E-mail: Jensen{at}caltech.edu or bc69{at}cornell.edu.
  • Author contributions: A.B., X.L., G.J.J., and B.R.C. designed research; A.B. and X.L. performed research; K.T.H. contributed new reagents/analytic tools; A.B., X.L., A.M.B., and B.R.C. analyzed data; and A.B., X.L., A.M.B., G.J.J., and B.R.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The atomic coordinates and structure factors have been deposited in the Protein Data Bank, www.pdb.org (PDB ID code 3UR1).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1115719109/-/DCSupplemental.

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Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins
Ariane Briegel, Xiaoxiao Li, Alexandrine M. Bilwes, Kelly T. Hughes, Grant J. Jensen, Brian R. Crane
Proceedings of the National Academy of Sciences Mar 2012, 109 (10) 3766-3771; DOI: 10.1073/pnas.1115719109

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Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins
Ariane Briegel, Xiaoxiao Li, Alexandrine M. Bilwes, Kelly T. Hughes, Grant J. Jensen, Brian R. Crane
Proceedings of the National Academy of Sciences Mar 2012, 109 (10) 3766-3771; DOI: 10.1073/pnas.1115719109
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Proceedings of the National Academy of Sciences: 109 (10)
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