A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide

Bacterial flagella mediate host–microbe interactions through tissue tropism during colonization, as well as by activating immune responses. The flagellar shaft of some bacteria, including several human pathogens, is encased in a membranous sheath of unknown function. While it has been hypothesized t...

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Main Authors: Caitlin A Brennan, Jason R Hunt, Natacha Kremer, Benjamin C Krasity, Michael A Apicella, Margaret J McFall-Ngai, Edward G Ruby
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/01579
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author Caitlin A Brennan
Jason R Hunt
Natacha Kremer
Benjamin C Krasity
Michael A Apicella
Margaret J McFall-Ngai
Edward G Ruby
author_facet Caitlin A Brennan
Jason R Hunt
Natacha Kremer
Benjamin C Krasity
Michael A Apicella
Margaret J McFall-Ngai
Edward G Ruby
author_sort Caitlin A Brennan
collection DOAJ
description Bacterial flagella mediate host–microbe interactions through tissue tropism during colonization, as well as by activating immune responses. The flagellar shaft of some bacteria, including several human pathogens, is encased in a membranous sheath of unknown function. While it has been hypothesized that the sheath may allow these bacteria to evade host responses to the immunogenic flagellin subunit, this unusual structural feature has remained an enigma. Here we demonstrate that the rotation of the sheathed flagellum in both the mutualist Vibrio fischeri and the pathogen Vibrio cholerae promotes release of a potent bacteria-derived immunogen, lipopolysaccharide, found in the flagellar sheath. We further present a new role for the flagellar sheath in triggering, rather than circumventing, host immune responses in the model squid-vibrio symbiosis. Such an observation not only has implications for the study of bacterial pathogens with sheathed flagella, but also raises important biophysical questions of sheathed-flagellum function.
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spelling doaj.art-d84ed2372c1f42f096c3ae95631b9cb12022-12-22T03:52:43ZengeLife Sciences Publications LtdeLife2050-084X2014-03-01310.7554/eLife.01579A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharideCaitlin A Brennan0Jason R Hunt1Natacha Kremer2Benjamin C Krasity3Michael A Apicella4Margaret J McFall-Ngai5Edward G Ruby6Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesDepartment of Microbiology, The Carver College of Medicine, University of Iowa, Iowa City, United States; Department of Internal Medicine, The Carver College of Medicine, University of Iowa, Iowa City, United StatesDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesDepartment of Microbiology, The Carver College of Medicine, University of Iowa, Iowa City, United States; Department of Internal Medicine, The Carver College of Medicine, University of Iowa, Iowa City, United StatesDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesBacterial flagella mediate host–microbe interactions through tissue tropism during colonization, as well as by activating immune responses. The flagellar shaft of some bacteria, including several human pathogens, is encased in a membranous sheath of unknown function. While it has been hypothesized that the sheath may allow these bacteria to evade host responses to the immunogenic flagellin subunit, this unusual structural feature has remained an enigma. Here we demonstrate that the rotation of the sheathed flagellum in both the mutualist Vibrio fischeri and the pathogen Vibrio cholerae promotes release of a potent bacteria-derived immunogen, lipopolysaccharide, found in the flagellar sheath. We further present a new role for the flagellar sheath in triggering, rather than circumventing, host immune responses in the model squid-vibrio symbiosis. Such an observation not only has implications for the study of bacterial pathogens with sheathed flagella, but also raises important biophysical questions of sheathed-flagellum function.https://elifesciences.org/articles/01579Vibrio fischericholeraeflagellaLPS
spellingShingle Caitlin A Brennan
Jason R Hunt
Natacha Kremer
Benjamin C Krasity
Michael A Apicella
Margaret J McFall-Ngai
Edward G Ruby
A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
eLife
Vibrio fischeri
cholerae
flagella
LPS
title A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
title_full A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
title_fullStr A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
title_full_unstemmed A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
title_short A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide
title_sort model symbiosis reveals a role for sheathed flagellum rotation in the release of immunogenic lipopolysaccharide
topic Vibrio fischeri
cholerae
flagella
LPS
url https://elifesciences.org/articles/01579
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