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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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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