The "Jack-of-all-Trades" Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral beta-Proteobacterium

Josie L. Ferreira; Izaak Coleman; Max L. Addison; Tobias Zachs; Bonnie L. Quigley; Kristin Wuichet; Morgan Beeby

doi:10.3389/fmicb.2021.643180

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The "Jack-of-all-Trades" Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral beta-Proteobacterium

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The "Jack-of-all-Trades" Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral beta-Proteobacterium

Josie L. Ferreira, Izaak Coleman, Max L. Addison, Tobias Zachs, Bonnie L. Quigley, Kristin Wuichet and Morgan Beeby

Frontiers in Microbiology, Vol.12, pp.1-8

2021

DOI: https://doi.org/10.3389/fmicb.2021.643180

PMID: 33859630

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Abstract

bacterial flagella

electron cryotomography

molecular evolution

subtomogram averaging

horizontal gene transfer

The gamma-proteobacteria are a group of diverse bacteria including pathogenic Escherichia, Salmonella, Vibrio, and Pseudomonas species. The majority swim in liquids with polar, sodium-driven flagella and swarm on surfaces with lateral, non-chemotactic flagella. Notable exceptions are the enteric Enterobacteriaceae such as Salmonella and E. coli. Many of the well-studied Enterobacteriaceae are gut bacteria that both swim and swarm with the same proton-driven peritrichous flagella. How different flagella evolved in closely related lineages, however, has remained unclear. Here, we describe our phylogenetic finding that Enterobacteriaceae flagella are not native polar or lateral gamma-proteobacterial flagella but were horizontally acquired from an ancestral beta-proteobacterium. Using electron cryo-tomography and subtomogram averaging, we confirmed that Enterobacteriaceae flagellar motors resemble contemporary beta-proteobacterial motors and are distinct to the polar and lateral motors of other gamma-proteobacteria. Structural comparisons support a model in which gamma-proteobacterial motors have specialized, suggesting that acquisition of a beta-proteobacterial flagellum may have been beneficial as a general-purpose motor suitable for adjusting to diverse conditions. This acquisition may have played a role in the development of the enteric lifestyle.

Details

Title: The "Jack-of-all-Trades" Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral beta-Proteobacterium
Authors: Josie L. Ferreira (Author) - Imperial College London
Izaak Coleman (Author) - Imperial Coll London, Dept Life Sci, London, England
Max L. Addison (Author) - Imperial College London
Tobias Zachs (Author) - Imperial College London
Bonnie L. Quigley (Author) - Imperial College London
Kristin Wuichet (Author) - Vanderbilt University Medical Center
Morgan Beeby (Corresponding Author) - Imperial College London
Publication details: Frontiers in Microbiology, Vol.12, pp.1-8; 8
Publisher: Frontiers Research Foundation
Date published: 2021
DOI: 10.3389/fmicb.2021.643180
ISSN: 1664-302X
PMID: 33859630
Copyright note: Copyright © 2021 Ferreira, Coleman, Addison, Zachs, Quigley, Wuichet and Beeby. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Grant note: MR/P019374/1 / Medical Research Council; UK Research & Innovation (UKRI); Medical Research Council UK (MRC); European Commission MR/K501281/1 / Medical Research Council Ph.D. Doctoral Training Partnership award BB/L023091/1 / BBSRC; UK Research & Innovation (UKRI); Biotechnology and Biological Sciences Research Council (BBSRC) 202596/Z/16/Z / Wellcome Trust; European Commission
Organisation Unit: University of the Sunshine Coast, Queensland; Thompson Institute; Centre for Bioinnovation
Language: English
Record Identifier: 99679198002621
Output Type: Journal article

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