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Research Article
Innate immune responses to gut microbiota differ between threespine stickleback populations
Kathryn Milligan-Myhre, Clayton M. Small, Erika K. Mittge, Meghna Agarwal, Mark Currey, William A. Cresko, Karen Guillemin
Disease Models & Mechanisms 2015 : dmm.021881 doi: 10.1242/dmm.021881 Published 17 December 2015
Kathryn Milligan-Myhre
Institute of Ecology and Evolution, University of Oregon, Eugene, OR, 97403, USAInstitute of Molecular Biology, University of Oregon, Eugene, OR, 97403, USABiological Science, University of Alaska Anchorage, Anchorage, AK, 99508, USA
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Clayton M. Small
Institute of Ecology and Evolution, University of Oregon, Eugene, OR, 97403, USA
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Erika K. Mittge
Institute of Molecular Biology, University of Oregon, Eugene, OR, 97403, USA
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Meghna Agarwal
Institute of Molecular Biology, University of Oregon, Eugene, OR, 97403, USA
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Mark Currey
Institute of Ecology and Evolution, University of Oregon, Eugene, OR, 97403, USA
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William A. Cresko
Institute of Ecology and Evolution, University of Oregon, Eugene, OR, 97403, USA
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Karen Guillemin
Institute of Molecular Biology, University of Oregon, Eugene, OR, 97403, USA
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Abstract

Animal hosts must co-exist with beneficial microbes while simultaneously being able to mount rapid, non-specific, innate immune responses to pathogenic microbes. How this balance is achieved is not fully understood, and disruption of this relationship can lead to disease. Excessive inflammatory responses to resident microbes are characteristic of certain gastrointestinal pathologies such as inflammatory bowel diseases (IBD). The immune dysregulation of IBD has complex genetic underpinnings that cannot be fully recapitulated with single gene knockout models. A deeper understanding of the genetic regulation of innate immune responses to resident microbes requires the ability to measure immune responses in the presence and absence of the microbiota using vertebrate models with complex genetic variation. Here we describe a new gnotobiotic vertebrate model to explore the natural genetic variation that contributes to differences in innate immune responses to microbiota. Threespine stickleback, Gasterosteus aculeatus, have been used to study the developmental genetics of complex traits during the repeated evolution from ancestral oceanic to derived freshwater forms. We established methods to rear germ-free stickleback larvae and gnotobiotic animals mono-associated with single bacterial isolates. We characterized the innate immune response of these fish to resident gut microbes by quantifying the neutrophil cells in conventionally reared, mono-associated, and germ-free stickleback from both oceanic and freshwater populations grown in a common intermediate salinity environment. We found that oceanic and freshwater fish in the wild and in the laboratory share many intestinal microbial community members. However, oceanic fish mount a strong immune response to residential microbiota whereas freshwater fish frequently do not. A strong innate immune response was uniformly observed across oceanic families, but this response varied among families of freshwater fish. The gnotobiotic stickleback model we have developed therefore provides a platform for future studies mapping the natural genetic basis of the variation in immune response to microbes.

  • Received June 11, 2015.
  • Accepted December 4, 2015.
  • © 2015. Published by The Company of Biologists Ltd

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Innate immune responses to gut microbiota differ between threespine stickleback populations
Kathryn Milligan-Myhre, Clayton M. Small, Erika K. Mittge, Meghna Agarwal, Mark Currey, William A. Cresko, Karen Guillemin
Disease Models & Mechanisms 2015 : dmm.021881 doi: 10.1242/dmm.021881 Published 17 December 2015
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Innate immune responses to gut microbiota differ between threespine stickleback populations
Kathryn Milligan-Myhre, Clayton M. Small, Erika K. Mittge, Meghna Agarwal, Mark Currey, William A. Cresko, Karen Guillemin
Disease Models & Mechanisms 2015 : dmm.021881 doi: 10.1242/dmm.021881 Published 17 December 2015

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