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

Briegel, Ariane and Li, Xiaoxiao and Bilwes, Alexandrine M. and Hughes, Kelly T. and Jensen, Grant J. and Crane, Brian R. (2012) Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proceedings of the National Academy of Sciences of the United States of America, 109 (10). pp. 3766-3771. ISSN 0027-8424. PMCID PMC3309718. doi:10.1073/pnas.1115719109. https://resolver.caltech.edu/CaltechAUTHORS:20120326-100949924

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1115719109DOIArticle
http://www.pnas.org/content/109/10/3766PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3309718/PubMed CentralArticle
ORCID:
AuthorORCID
Briegel, Ariane0000-0003-3733-3725
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2012 National Academy of Sciences. Edited by Laura L. Kiessling, University of Wisconsin, Madison, WI, and approved January 13, 2012 (received for review September 23, 2011). 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. We thank Drs. Morgan Beeby and Songye Chen for collecting some of the tomographic data, Dr. John Heumann for help using the PEET software, Dr. Stanley Maloy for suggesting FtsZ overexpression for minicell production, and A. Vu and Dr. F.W. Dahlquist for advice on choosing constructs for crystallization. We also thank the Cornell High Energy Synchrotron Source for access to data collection facilities. This work was supported by the Howard Hughes Medical Institute, by gifts to Caltech from The Gordon and Betty Moore Foundation, and by National Institutes of Health Grant GM066775 (to B.R.C.).
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
NIHGM066775
Issue or Number:10
PubMed Central ID:PMC3309718
DOI:10.1073/pnas.1115719109
Record Number:CaltechAUTHORS:20120326-100949924
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20120326-100949924
Official Citation: Ariane Briegel, Xiaoxiao Li, Alexandrine M. Bilwes, Kelly T. Hughes, Grant J. Jensen, and Brian R. Crane Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins PNAS 2012 109 (10) 3766-3771; published ahead of print February 21, 2012, doi:10.1073/pnas.1115719109
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:29841
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:26 Mar 2012 17:42
Last Modified:09 Nov 2021 19:31

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