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Bacterial flagellar motor PL-ring disassembly subcomplexes are widespread and ancient

Kaplan, Mohammed and Sweredoski, Michael J. and Rodrigues, João P. G. L. M. and Tocheva, Elitza I. and Chang, Yi-Wei and Ortega, Davi R. and Beeby, Morgan and Jensen, Grant J. (2020) Bacterial flagellar motor PL-ring disassembly subcomplexes are widespread and ancient. Proceedings of the National Academy of Sciences of the United States of America, 117 (16). pp. 8941-8947. ISSN 0027-8424. PMCID PMC7183148. https://resolver.caltech.edu/CaltechAUTHORS:20200403-104455365

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Abstract

The bacterial flagellum is an amazing nanomachine. Understanding how such complex structures arose is crucial to our understanding of cellular evolution. We and others recently reported that in several Gammaproteobacterial species, a relic subcomplex comprising the decorated P and L rings persists in the outer membrane after flagellum disassembly. Imaging nine additional species with cryo-electron tomography, here, we show that this subcomplex persists after flagellum disassembly in other phyla as well. Bioinformatic analyses fail to show evidence of any recent horizontal transfers of the P- and L-ring genes, suggesting that this subcomplex and its persistence is an ancient and conserved feature of the flagellar motor. We hypothesize that one function of the P and L rings is to seal the outer membrane after motor disassembly.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1916935117DOIArticle
https://www.pnas.org/content/suppl/2020/04/01/1916935117.DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183148PubMed CentralArticle
ORCID:
AuthorORCID
Kaplan, Mohammed0000-0002-0759-0459
Sweredoski, Michael J.0000-0003-0878-3831
Tocheva, Elitza I.0000-0002-4869-8319
Chang, Yi-Wei0000-0003-2391-473X
Ortega, Davi R.0000-0002-8344-2335
Beeby, Morgan0000-0001-6413-9835
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2020 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Jody W. Deming, University of Washington, Seattle, WA, and approved February 24, 2020 (received for review September 28, 2019). PNAS first published April 2, 2020. This work was supported by NIH Grant R35 GM122588 (to G.J.J.). Cryo-ET work was done in the Beckman Institute Resource Center for Transmission Electron Microscopy at the California Institute of Technology. M.K. was supported by a Rubicon postdoctoral fellowship from De Nederlandse Organisatie voor Wetenschappelijk Onderzoek. J.P.G.L.M.R. was supported by NIH Grant R35GM122543. Ariane Briegel kindly helped in collecting part of the data. We thank Catherine M. Oikonomou for reading the manuscript and for the insightful discussions; and Dr. Pat Zambryski from the University of California, Berkeley for providing us with the A. longum strain used in this study. Data Availability: Some of the data used in this study are available in the Electron Tomography Database (ETDB)-Caltech (48). All of the data are available upon request from the corresponding author. Author contributions: M.K. and G.J.J. designed research; M.K., M.J.S., J.P.G.L.M.R., E.I.T., Y.-W.C., D.R.O., and M.B. performed research; M.K. and G.J.J. contributed new reagents/analytic tools; M.K., M.J.S., and G.J.J. analyzed data; and M.K. and G.J.J. wrote the paper. The authors declare no competing interest. This article is a PNAS Direct Submission. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1916935117/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NIHR35 GM122588
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)UNSPECIFIED
NIHR35GM122543
Subject Keywords:cryo-electron tomography; flagellar motor; evolution
Issue or Number:16
PubMed Central ID:PMC7183148
Record Number:CaltechAUTHORS:20200403-104455365
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200403-104455365
Official Citation:Bacterial flagellar motor PL-ring disassembly subcomplexes are widespread and ancient. Mohammed Kaplan, Michael J. Sweredoski, João P. G. L. M. Rodrigues, Elitza I. Tocheva, Yi-Wei Chang, Davi R. Ortega, Morgan Beeby, Grant J. Jensen. Proceedings of the National Academy of Sciences Apr 2020, 117 (16) 8941-8947; DOI: 10.1073/pnas.1916935117
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:102314
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:03 Apr 2020 17:58
Last Modified:01 May 2020 15:49

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