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Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome
BACKGROUND: Salmonella is one of the most significant food-borne pathogens to affect humans and agriculture. While it is well documented that Salmonella infection triggers host inflammation, the impacts on the gut environment are largely unknown. A CBA/J mouse model was used to evaluate intestinal r...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5408407/ https://www.ncbi.nlm.nih.gov/pubmed/28449706 http://dx.doi.org/10.1186/s40168-017-0264-8 |
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author | Borton, Mikayla A. Sabag-Daigle, Anice Wu, Jikang Solden, Lindsey M. O’Banion, Bridget S. Daly, Rebecca A. Wolfe, Richard A. Gonzalez, Juan F. Wysocki, Vicki H. Ahmer, Brian M. M. Wrighton, Kelly C. |
author_facet | Borton, Mikayla A. Sabag-Daigle, Anice Wu, Jikang Solden, Lindsey M. O’Banion, Bridget S. Daly, Rebecca A. Wolfe, Richard A. Gonzalez, Juan F. Wysocki, Vicki H. Ahmer, Brian M. M. Wrighton, Kelly C. |
author_sort | Borton, Mikayla A. |
collection | PubMed |
description | BACKGROUND: Salmonella is one of the most significant food-borne pathogens to affect humans and agriculture. While it is well documented that Salmonella infection triggers host inflammation, the impacts on the gut environment are largely unknown. A CBA/J mouse model was used to evaluate intestinal responses to Salmonella-induced inflammation. In parallel, we evaluated chemically induced inflammation by dextran sodium sulfate (DSS) and a non-inflammation control. We profiled gut microbial diversity by sequencing 16S ribosomal ribonucleic acid (rRNA) genes from fecal and cecal samples. These data were correlated to the inflammation marker lipocalin-2 and short-chain fatty acid concentrations. RESULTS: We demonstrated that inflammation, chemically or biologically induced, restructures the chemical and microbial environment of the gut over a 16-day period. We observed that the ten mice within the Salmonella treatment group had a variable Salmonella relative abundance, with three high responding mice dominated by >46% Salmonella at later time points and the remaining seven mice denoted as low responders. These low- and high-responding Salmonella groups, along with the chemical DSS treatment, established an inflammation gradient with chemical and low levels of Salmonella having at least 3 log-fold lower lipocalin-2 concentration than the high-responding Salmonella mice. Total short-chain fatty acid and individual butyrate concentrations each negatively correlated with inflammation levels. Microbial communities were also structured along this inflammation gradient. Low levels of inflammation, regardless of chemical or biological induction, enriched for Akkermansia spp. in the Verrucomicrobiaceae and members of the Bacteroidetes family S24-7. Relative to the control or low inflammation groups, high levels of Salmonella drastically decreased the overall microbial diversity, specifically driven by the reduction of Alistipes and Lachnospiraceae in the Bacteroidetes and Firmicutes phyla, respectively. Conversely, members of the Enterobacteriaceae and Lactobacillus were positively correlated to high levels of Salmonella-induced inflammation. CONCLUSIONS: Our results show that enteropathogenic infection and intestinal inflammation are interrelated factors modulating gut homeostasis. These findings may prove informative with regard to prophylactic or therapeutic strategies to prevent disruption of microbial communities, or promote their restoration. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-017-0264-8) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-5408407 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-54084072017-05-02 Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome Borton, Mikayla A. Sabag-Daigle, Anice Wu, Jikang Solden, Lindsey M. O’Banion, Bridget S. Daly, Rebecca A. Wolfe, Richard A. Gonzalez, Juan F. Wysocki, Vicki H. Ahmer, Brian M. M. Wrighton, Kelly C. Microbiome Research BACKGROUND: Salmonella is one of the most significant food-borne pathogens to affect humans and agriculture. While it is well documented that Salmonella infection triggers host inflammation, the impacts on the gut environment are largely unknown. A CBA/J mouse model was used to evaluate intestinal responses to Salmonella-induced inflammation. In parallel, we evaluated chemically induced inflammation by dextran sodium sulfate (DSS) and a non-inflammation control. We profiled gut microbial diversity by sequencing 16S ribosomal ribonucleic acid (rRNA) genes from fecal and cecal samples. These data were correlated to the inflammation marker lipocalin-2 and short-chain fatty acid concentrations. RESULTS: We demonstrated that inflammation, chemically or biologically induced, restructures the chemical and microbial environment of the gut over a 16-day period. We observed that the ten mice within the Salmonella treatment group had a variable Salmonella relative abundance, with three high responding mice dominated by >46% Salmonella at later time points and the remaining seven mice denoted as low responders. These low- and high-responding Salmonella groups, along with the chemical DSS treatment, established an inflammation gradient with chemical and low levels of Salmonella having at least 3 log-fold lower lipocalin-2 concentration than the high-responding Salmonella mice. Total short-chain fatty acid and individual butyrate concentrations each negatively correlated with inflammation levels. Microbial communities were also structured along this inflammation gradient. Low levels of inflammation, regardless of chemical or biological induction, enriched for Akkermansia spp. in the Verrucomicrobiaceae and members of the Bacteroidetes family S24-7. Relative to the control or low inflammation groups, high levels of Salmonella drastically decreased the overall microbial diversity, specifically driven by the reduction of Alistipes and Lachnospiraceae in the Bacteroidetes and Firmicutes phyla, respectively. Conversely, members of the Enterobacteriaceae and Lactobacillus were positively correlated to high levels of Salmonella-induced inflammation. CONCLUSIONS: Our results show that enteropathogenic infection and intestinal inflammation are interrelated factors modulating gut homeostasis. These findings may prove informative with regard to prophylactic or therapeutic strategies to prevent disruption of microbial communities, or promote their restoration. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-017-0264-8) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-27 /pmc/articles/PMC5408407/ /pubmed/28449706 http://dx.doi.org/10.1186/s40168-017-0264-8 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Borton, Mikayla A. Sabag-Daigle, Anice Wu, Jikang Solden, Lindsey M. O’Banion, Bridget S. Daly, Rebecca A. Wolfe, Richard A. Gonzalez, Juan F. Wysocki, Vicki H. Ahmer, Brian M. M. Wrighton, Kelly C. Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title | Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title_full | Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title_fullStr | Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title_full_unstemmed | Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title_short | Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
title_sort | chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5408407/ https://www.ncbi.nlm.nih.gov/pubmed/28449706 http://dx.doi.org/10.1186/s40168-017-0264-8 |
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