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Discovery of a Novel Inner Membrane-Associated Bacterial Structure Related to the Flagellar Type III Secretion System

Kaplan, Mohammed and Oikonomou, Catherine M. and Wood, Cecily R. and Chreifi, Georges and Ghosal, Debnath and Dobro, Megan J. and Yao, Qing and Pal, Ritesh Ranjan and Baidya, Amit K. and Liu, Yuxi and Maggi, Stefano and McDowall, Alasdair W. and Ben-Yehuda, Sigal and Rosenshine, Ilan and Briegel, Ariane and Beeby, Morgan and Chang, Yi-Wei and Shaffer, Carrie L. and Jensen, Grant J. (2022) Discovery of a Novel Inner Membrane-Associated Bacterial Structure Related to the Flagellar Type III Secretion System. Journal of Bacteriology, 204 (8). Art. No. jb.00144-22. ISSN 0021-9193. doi:10.1128/jb.00144-22. https://resolver.caltech.edu/CaltechAUTHORS:20220729-894327000

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Abstract

The bacterial flagellar type III secretion system (fT3SS) is a suite of membrane-embedded and cytoplasmic proteins responsible for building the flagellar motility machinery. Homologous nonflagellar (NF-T3SS) proteins form the injectisome machinery that bacteria use to deliver effector proteins into eukaryotic cells, and other family members were recently reported to be involved in the formation of membrane nanotubes. Here, we describe a novel, evolutionarily widespread, hat-shaped structure embedded in the inner membranes of bacteria, of yet-unidentified function, that is present in species containing fT3SS. Mutant analysis suggests a relationship between this novel structure and the fT3SS, but not the NF-T3SS. While the function of this novel structure remains unknown, we hypothesize that either some of the fT3SS proteins assemble within the hat-like structure, perhaps including the fT3SS core complex, or that fT3SS components regulate other proteins that form part of this novel structure.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/jb.00144-22DOIArticle
https://journals.asm.org/doi/suppl/10.1128/jb.00144-22/suppl_file/jb.00144-22-s0001.pdfPublisherSupporting Information
https://journals.asm.org/doi/suppl/10.1128/jb.00144-22/suppl_file/jb.00144-22-s0002.movPublisherSupporting Information
ORCID:
AuthorORCID
Kaplan, Mohammed0000-0002-0759-0459
Oikonomou, Catherine M.0000-0003-2312-4746
Wood, Cecily R.0000-0003-1259-3862
Chreifi, Georges0000-0003-4194-1694
Ghosal, Debnath0000-0002-2227-0330
Dobro, Megan J.0000-0002-6464-3932
Yao, Qing0000-0003-3575-9909
Pal, Ritesh Ranjan0000-0002-7513-6792
Liu, Yuxi0000-0003-1439-9000
Briegel, Ariane0000-0003-3733-3725
Beeby, Morgan0000-0001-6413-9835
Chang, Yi-Wei0000-0003-2391-473X
Shaffer, Carrie L.0000-0002-7457-7422
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2022 Kaplan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received: 19 April 2022. Accepted: 30 May 2022. Published online: 18 July 2022. This project was funded by the NIH (grant R01 AI127401 to G.J.J., and grant P20 GM130456 to C.L.S.) and the European Research Council (ERC) Synergy grant (no. 810186 awarded to S.B.Y. and I.R.). M.K. acknowledges a Baxter postdoctoral fellowship from Caltech. Cryo-ET work was done in the Beckman Institute Resource Center for Transmission Electron Microscopy at the California Institute of Technology. We are grateful to Marc Erhardt (Humboldt-Universität zu Berlin) for critically reading an initial version of this work. We thank Elitza I. Tocheva for collecting the A. tumefaciens data, Jian Shi for collecting the H. neptunium data, and Martin Pilhofer for collecting the P. luteoviolacea data. We thank Dianne Newman’s lab for providing the P. aeruginosa transposon mutant. We are grateful to the lab of Robert Heinzen at the National Institute of Allergy and Infectious Diseases in Montana for growing the Coxiella burnetii cells. The authors declare no conflict of interest.
Funders:
Funding AgencyGrant Number
NIHR01 AI127401
NIHP20 GM130456
European Research Council (ERC)810186
Baxter FoundationUNSPECIFIED
Subject Keywords:bacteria; cryo-ET; flagella; secretion systems
Issue or Number:8
DOI:10.1128/jb.00144-22
Record Number:CaltechAUTHORS:20220729-894327000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220729-894327000
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:115975
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Aug 2022 22:44
Last Modified:24 Aug 2022 22:22

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