A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish

Stable mutualism between a host and its resident bacteria requires a moderated immune response to control bacterial population size without eliciting excessive inflammation that could harm both partners. Little is known about the specific molecular mechanisms utilized by bacterial mutualists to temp...

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Main Authors: Annah S Rolig, Emily Goers Sweeney, Lila E Kaye, Michael D DeSantis, Arden Perkins, Allison V Banse, M Kristina Hamilton, Karen Guillemin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/37172
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spelling doaj-a485b9400d2a40598196c1195f2cc15f2021-05-05T16:16:02ZengeLife Sciences Publications LtdeLife2050-084X2018-11-01710.7554/eLife.37172A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafishAnnah S Rolig0https://orcid.org/0000-0001-7080-4352Emily Goers Sweeney1https://orcid.org/0000-0002-5539-8875Lila E Kaye2Michael D DeSantis3Arden Perkins4Allison V Banse5M Kristina Hamilton6Karen Guillemin7https://orcid.org/0000-0001-6004-9955Institute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United StatesInstitute of Neuroscience, University of Oregon, Eugene, United StatesInstitute of Molecular Biology, University of Oregon, Eugene, United States; Humans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, CanadaStable mutualism between a host and its resident bacteria requires a moderated immune response to control bacterial population size without eliciting excessive inflammation that could harm both partners. Little is known about the specific molecular mechanisms utilized by bacterial mutualists to temper their hosts’ responses and protect themselves from aggressive immune attack. Using a gnotobiotic larval zebrafish model, we identified an Aeromonas secreted immunomodulatory protein, AimA. AimA is required during colonization to prevent intestinal inflammation that simultaneously compromises both bacterial and host survival. Administration of exogenous AimA prevents excessive intestinal neutrophil accumulation and protects against septic shock in models of both bacterially and chemically induced intestinal inflammation. We determined the molecular structure of AimA, which revealed two related calycin-like domains with structural similarity to the mammalian immune modulatory protein, lipocalin-2. As a secreted bacterial protein required by both partners for optimal fitness, AimA is an exemplar bacterial mutualism factor.https://elifesciences.org/articles/37172inflammationmicrobiotazebrafishlipocalinAeromonasmutualism
collection DOAJ
language English
format Article
sources DOAJ
author Annah S Rolig
Emily Goers Sweeney
Lila E Kaye
Michael D DeSantis
Arden Perkins
Allison V Banse
M Kristina Hamilton
Karen Guillemin
spellingShingle Annah S Rolig
Emily Goers Sweeney
Lila E Kaye
Michael D DeSantis
Arden Perkins
Allison V Banse
M Kristina Hamilton
Karen Guillemin
A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
eLife
inflammation
microbiota
zebrafish
lipocalin
Aeromonas
mutualism
author_facet Annah S Rolig
Emily Goers Sweeney
Lila E Kaye
Michael D DeSantis
Arden Perkins
Allison V Banse
M Kristina Hamilton
Karen Guillemin
author_sort Annah S Rolig
title A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
title_short A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
title_full A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
title_fullStr A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
title_full_unstemmed A bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
title_sort bacterial immunomodulatory protein with lipocalin-like domains facilitates host–bacteria mutualism in larval zebrafish
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-11-01
description Stable mutualism between a host and its resident bacteria requires a moderated immune response to control bacterial population size without eliciting excessive inflammation that could harm both partners. Little is known about the specific molecular mechanisms utilized by bacterial mutualists to temper their hosts’ responses and protect themselves from aggressive immune attack. Using a gnotobiotic larval zebrafish model, we identified an Aeromonas secreted immunomodulatory protein, AimA. AimA is required during colonization to prevent intestinal inflammation that simultaneously compromises both bacterial and host survival. Administration of exogenous AimA prevents excessive intestinal neutrophil accumulation and protects against septic shock in models of both bacterially and chemically induced intestinal inflammation. We determined the molecular structure of AimA, which revealed two related calycin-like domains with structural similarity to the mammalian immune modulatory protein, lipocalin-2. As a secreted bacterial protein required by both partners for optimal fitness, AimA is an exemplar bacterial mutualism factor.
topic inflammation
microbiota
zebrafish
lipocalin
Aeromonas
mutualism
url https://elifesciences.org/articles/37172
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