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Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output

O’Neal, Lindsey and Gullett, Jessica M. and Aksenova, Anastasia and Hubler, Adam and Briegel, Ariane and Ortega, Davi and Kjær, Andreas and Jensen, Grant and Alexandre, Gladys (2019) Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output. mBio, 10 (5). Art. No. e01757-19. ISSN 2150-7511. PMCID PMC6759762. https://resolver.caltech.edu/CaltechAUTHORS:20190924-095952844

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Abstract

Most chemotactic motile bacteria possess multiple chemotaxis signaling systems, the functions of which are not well characterized. Chemotaxis signaling is initiated by chemoreceptors that assemble as large arrays, together with chemotaxis coupling proteins (CheW) and histidine kinase proteins (CheA), which form a baseplate with the cytoplasmic tips of receptors. These cell pole-localized arrays mediate sensing, signaling, and signal amplification during chemotaxis responses. Membrane-bound chemoreceptors with different cytoplasmic domain lengths segregate into distinct arrays. Here, we show that a bacterium, Azospirillum brasilense, which utilizes two chemotaxis signaling systems controlling distinct motility parameters, coordinates its chemotactic responses through the production of two separate membrane-bound chemoreceptor arrays by mixing paralogs within chemotaxis baseplates. The polar localization of chemoreceptors of different length classes is maintained in strains that had baseplate signaling proteins from either chemotaxis system but was lost when both systems were deleted. Chemotaxis proteins (CheA and CheW) from each of the chemotaxis signaling systems (Che1 and Che4) could physically interact with one another, and chemoreceptors from both classes present in A. brasilense could interact with Che1 and Che4 proteins. The assembly of paralogs from distinct chemotaxis pathways into baseplates provides a straightforward mechanism for coordinating signaling from distinct pathways, which we predict is not unique to this system given the propensity of chemotaxis systems for horizontal gene transfer.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mbio.01757-19DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6759762/PubMed CentralArticle
ORCID:
AuthorORCID
Briegel, Ariane0000-0003-3733-3725
Ortega, Davi0000-0002-8344-2335
Kjær, Andreas0000-0002-0096-5764
Jensen, Grant0000-0003-1556-4864
Alexandre, Gladys0000-0002-9238-4640
Additional Information:© 2019 O’Neal et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 9 July 2019; Accepted 27 August 2019; Published 24 September 2019. We thank Lam Vo for excellent technical assistance. This research was supported by National Science Foundation grants NSF-MCB 1330344 and NSF-MCB 1715185 (to G.A.). Any opinions, findings, conclusions, or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
Funders:
Funding AgencyGrant Number
NSFMCB-1330344
NSFMCB-1715185
Issue or Number:5
PubMed Central ID:PMC6759762
Record Number:CaltechAUTHORS:20190924-095952844
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190924-095952844
Official Citation:O’Neal L, Gullett JM, Aksenova A, Hubler A, Briegel A, Ortega D, Kjær A, Jensen G, Alexandre G. 2019. Distinct chemotaxis protein paralogs assemble into chemoreceptor signaling arrays to coordinate signaling output. mBio 10:e01757-19. https://doi.org/10.1128/ mBio.01757-19.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98828
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:24 Sep 2019 17:13
Last Modified:04 Oct 2019 21:45

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