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Atypical chemoreceptor arrays accommodate high membrane curvature

Muok, Alise R. and Ortega, Davi R. and Kurniyati, Kurni and Yang, Wen and Maschmann, Zachary A. and Sidi Mabrouk, Adam and Li, Chunhao and Crane, Brian R. and Briegel, Ariane (2020) Atypical chemoreceptor arrays accommodate high membrane curvature. Nature Communications, 11 . Art. No. 5763. ISSN 2041-1723. https://resolver.caltech.edu/CaltechAUTHORS:20200313-142323198

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Abstract

The prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology. In all previously described species, chemoreceptors organize into a hexagonal (P6 symmetry) extended array. Here, we report an alternative symmetry (P2) of the chemotaxis apparatus that emerges from a strict linear organization of the histidine kinase CheA in Treponema denticola cells, which possesses arrays with the highest native curvature investigated thus far. Using cryo-ET, we reveal that Td chemoreceptor arrays assume an unusual arrangement of the supra-molecular protein assembly that has likely evolved to accommodate the high membrane curvature. The arrays have several atypical features, such as an extended dimerization domain of CheA and a variant CheW-CheR-like fusion protein that is critical for maintaining an ordered chemosensory apparatus. Furthermore, the previously characterized Td oxygen sensor ODP influences CheA ordering. These results suggest a greater diversity of the chemotaxis signaling system than previously thought.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-020-19628-6DOIArticle
https://doi.org/10.1101/2020.03.11.986844DOIDiscussion Paper
https://gitlab.com/lab-notebook/treponemaRelated ItemCode
ORCID:
AuthorORCID
Muok, Alise R.0000-0001-8695-3221
Ortega, Davi R.0000-0002-8344-2335
Maschmann, Zachary A.0000-0002-7938-0792
Sidi Mabrouk, Adam0000-0002-7000-0386
Li, Chunhao0000-0002-1872-4870
Crane, Brian R.0000-0001-8234-9991
Briegel, Ariane0000-0003-3733-3725
Alternate Title:Spirochetes produce ordered chemoreceptor arrays of unusual composition, arrangement, and symmetry to compensate for a highly curved membrane
Additional Information:© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 04 April 2020; Accepted 23 October 2020; Published 13 November 2020. We thank Alister Burt (Universite Grenoble Alpes), Dr. Frederic Bonnet (Netherlands Centre for Electron Nanoscopy, NeCEN), and Dr. Ludovic Renault (NeCEN) for assistance with processing of the sub-tomogram averages. We also thank Dr. Robbert Q. Kim at the Leiden University Medical Center (LUMC) Protein Facility for help with the ITC experiments, and Dr. Elena Domínguez-Vega and Prof. Manfred Wuhrer for the native MS analysis. This work is part of the research program National Roadmap for Large-Scale Research Infrastructure 2017–2018 with project number 184.034.014, which is financed in part by the Dutch Research Council (NWO). This work was funded by a grant from the National Institutes of Health: R35GM122535 awarded to B.R.C., R01AI078958 and R01DE023080 to C.L., and by the European Union under a Marie-Sklodowska-Curie COFUND LEaDing fellowship to ARM. We thank the Netherlands Centre for Electron Nanoscopy (NeCEN) for access to cryo-ET data collection facilities, and NE-CAT at the Advanced Photon Source for access to x-ray crystallography data collection facilities. NE-CAT is supported by NIH/NIGMS awards P30 GM124165 and S10 RR029205. Data availability: Data supporting the findings of this manuscript are available from the corresponding author upon reasonable request. A reporting summary for this Article is available as a Supplementary Information file. The cryo-ET sub-tomogram averages that support these findings are deposited in the Electron Microscopy Data Bank (EMDB) with accession codes EMD-11385, EMD-11381, EMD-11384, and EMD-11386. The protein x-ray crystallography structure that supports these findings is deposited in the Protein Data Bank (PDB) with accession code 6Y1Y. The sub-tomogram average pictured in Figure. 1c, d is derived from a public repository (EMD-4991)25. Source data are provided with this paper. Code availability: All custom-made scripts and instructions on how to reproduce the bioinformatics data are available on GitLab (https://gitlab.com/lab-notebook/treponema). Author Contributions: A.R.M., D.R.O., K.K., Z.A.M., C.L., B.R.C., and A.B. designed research; A.R.M., D.R.O., K.K., and Z.A.M. performed research; A.R.M., D.R.O., W.Y., K.K., Z.A.M., and A.S. analyzed data; and A.R.M., D.R.O., and A.B. wrote the paper with input from all authors. The authors declare no competing interests. Peer review information: Nature Communications thanks Tino Krell, Mikhail Kudryashev, and other, anonymous, reviewers for their contributions to the peer review of this work. Peer review reports are available.
Funders:
Funding AgencyGrant Number
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)184.034.014
NIHR35GM122535
NIHR01AI078958
NIHR01DE023080
Marie Curie FellowshipUNSPECIFIED
NIHP30 GM124165
NIHS10 RR029205
Subject Keywords:Bacteria; Cryoelectron tomography; Microbiology
Record Number:CaltechAUTHORS:20200313-142323198
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200313-142323198
Official Citation:Muok, A.R., Ortega, D.R., Kurniyati, K. et al. Atypical chemoreceptor arrays accommodate high membrane curvature. Nat Commun 11, 5763 (2020). https://doi.org/10.1038/s41467-020-19628-6
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:101912
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:16 Mar 2020 14:01
Last Modified:16 Nov 2020 23:51

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