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Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling

Briegel, Ariane and Ladinsky, Mark S. and Oikonomou, Catherine M. and Jones, Christopher W. and Harris, Michael J. and Fowler, Daniel J. and Chang, Yi-Wei and Thompson, Lynmarie K. and Armitage, Judith P. and Jensen, Grant J. (2014) Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling. eLife, 3 . Art. No. e02151. ISSN 2050-084X. PMCID PMC3964821. https://resolver.caltech.edu/CaltechAUTHORS:20140502-092924910

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Abstract

Most motile bacteria sense and respond to their environment through a transmembrane chemoreceptor array whose structure and function have been well-studied, but many species also contain an additional cluster of chemoreceptors in their cytoplasm. Although the cytoplasmic cluster is essential for normal chemotaxis in some organisms, its structure and function remain unknown. Here we use electron cryotomography to image the cytoplasmic chemoreceptor cluster in Rhodobacter sphaeroides and Vibrio cholerae. We show that just like transmembrane arrays, cytoplasmic clusters contain trimers-of-receptor-dimers organized in 12-nm hexagonal arrays. In contrast to transmembrane arrays, however, cytoplasmic clusters comprise two CheA/ CheW baseplates sandwiching two opposed receptor arrays. We further show that cytoplasmic fragments of normally transmembrane E. coli chemoreceptors form similar sandwiched structures in the presence of molecular crowding agents. Together these results suggest that the 12-nm hexagonal architecture is fundamentally important and that sandwiching and crowding can replace the stabilizing effect of the membrane.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.7554/eLife.02151.001DOIArticle
http://elifesciences.org/content/3/e02151/abstract-1PublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3964821/PubMed CentralArticle
ORCID:
AuthorORCID
Briegel, Ariane0000-0003-3733-3725
Ladinsky, Mark S.0000-0002-1036-3513
Oikonomou, Catherine M.0000-0003-2312-4746
Chang, Yi-Wei0000-0003-2391-473X
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2014 Briegel et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 21 December 2013; Accepted: 20 February 2014; Published: 25 March 2014. The authors wish to thank Lee Rettberg and Audrey Huang for experimental help, and Dr Matthew Waldor for kindly providing strain MKW1383. Special thanks to Drs Zhiheng Yu and Jason de la Cruz for microscopy support at HHMI Janelia Farms. JPA and CWJ thank BBSRC and Nikon for funding. This work was additionally supported by NIH grant R01-GM085288 to LKT and NIGMS grant GM101425 to GJJ.
Funders:
Funding AgencyGrant Number
NIHGM101425
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIHR01-GM085288
Biotechnology and Biological Sciences Research Council (BBSRC)UNSPECIFIED
NikonUNSPECIFIED
National Institute of General Medical SciencesUNSPECIFIED
PubMed Central ID:PMC3964821
Record Number:CaltechAUTHORS:20140502-092924910
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140502-092924910
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:45460
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:05 May 2014 17:53
Last Modified:05 Nov 2019 21:04

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