Cargando…

Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota

BACKGROUND: The microbiota of the mammalian gastrointestinal (GI) tract consists of diverse populations of commensal bacteria that interact with host physiological function. Dysregulating these populations, through exogenous means such as antibiotics or dietary changes, can have adverse consequences...

Descripción completa

Detalles Bibliográficos
Autores principales: Galley, Jeffrey D, Nelson, Michael C, Yu, Zhongtang, Dowd, Scot E, Walter, Jens, Kumar, Purnima S, Lyte, Mark, Bailey, Michael T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4105248/
https://www.ncbi.nlm.nih.gov/pubmed/25028050
http://dx.doi.org/10.1186/1471-2180-14-189
_version_ 1782327338484105216
author Galley, Jeffrey D
Nelson, Michael C
Yu, Zhongtang
Dowd, Scot E
Walter, Jens
Kumar, Purnima S
Lyte, Mark
Bailey, Michael T
author_facet Galley, Jeffrey D
Nelson, Michael C
Yu, Zhongtang
Dowd, Scot E
Walter, Jens
Kumar, Purnima S
Lyte, Mark
Bailey, Michael T
author_sort Galley, Jeffrey D
collection PubMed
description BACKGROUND: The microbiota of the mammalian gastrointestinal (GI) tract consists of diverse populations of commensal bacteria that interact with host physiological function. Dysregulating these populations, through exogenous means such as antibiotics or dietary changes, can have adverse consequences on the health of the host. Studies from laboratories such as ours have demonstrated that exposure to psychological stressors disrupts the population profile of intestinal microbiota. To date, such studies have primarily focused on prolonged stressors (repeated across several days) and have assessed fecal bacterial populations. It is not known whether shorter stressors can also impact the microbiota, and whether colonic mucosa-associated populations can also be affected. The mucosa-associated microbiota exist in close proximity to elements of the host immune system and the two are tightly interrelated. Therefore, alterations in these populations should be emphasized. Additionally, stressors can induce differential responses in anxiety-like behavior and corticosterone outputs in variant strains of mice. Thus, whether stressor exposure can have contrasting effects on the colonic microbiota in inbred C57BL/6 mice and outbred CD-1 mice was also examined. RESULTS: In the present study, we used high throughput pyrosequencing to assess the effects of a single 2-hour exposure to a social stressor, called social disruption (SDR), on colonic mucosa-associated microbial profiles of C57BL/6 mice. The data indicate that exposure to the stressor significantly changed the community profile and significantly reduced the relative proportions of two genera and one family of highly abundant intestinal bacteria, including the genus Lactobacillus. This finding was confirmed using a quantitative real-time polymerase chain reaction (qPCR) technique. The use of qPCR also identified mouse strain-specific differences in bacterial abundances. L. reuteri, an immunomodulatory species, was decreased in stressor-exposed CD-1 mice, but not C57BL/6 mice. CONCLUSIONS: These data illustrate that stressor exposure can affect microbial populations, including the lactobacilli, that are closely associated with the colonic mucosa. Because the lactobacilli can have beneficial effects on human health, stressor-induced reductions of their population could have important health implications.
format Online
Article
Text
id pubmed-4105248
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-41052482014-07-22 Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota Galley, Jeffrey D Nelson, Michael C Yu, Zhongtang Dowd, Scot E Walter, Jens Kumar, Purnima S Lyte, Mark Bailey, Michael T BMC Microbiol Research Article BACKGROUND: The microbiota of the mammalian gastrointestinal (GI) tract consists of diverse populations of commensal bacteria that interact with host physiological function. Dysregulating these populations, through exogenous means such as antibiotics or dietary changes, can have adverse consequences on the health of the host. Studies from laboratories such as ours have demonstrated that exposure to psychological stressors disrupts the population profile of intestinal microbiota. To date, such studies have primarily focused on prolonged stressors (repeated across several days) and have assessed fecal bacterial populations. It is not known whether shorter stressors can also impact the microbiota, and whether colonic mucosa-associated populations can also be affected. The mucosa-associated microbiota exist in close proximity to elements of the host immune system and the two are tightly interrelated. Therefore, alterations in these populations should be emphasized. Additionally, stressors can induce differential responses in anxiety-like behavior and corticosterone outputs in variant strains of mice. Thus, whether stressor exposure can have contrasting effects on the colonic microbiota in inbred C57BL/6 mice and outbred CD-1 mice was also examined. RESULTS: In the present study, we used high throughput pyrosequencing to assess the effects of a single 2-hour exposure to a social stressor, called social disruption (SDR), on colonic mucosa-associated microbial profiles of C57BL/6 mice. The data indicate that exposure to the stressor significantly changed the community profile and significantly reduced the relative proportions of two genera and one family of highly abundant intestinal bacteria, including the genus Lactobacillus. This finding was confirmed using a quantitative real-time polymerase chain reaction (qPCR) technique. The use of qPCR also identified mouse strain-specific differences in bacterial abundances. L. reuteri, an immunomodulatory species, was decreased in stressor-exposed CD-1 mice, but not C57BL/6 mice. CONCLUSIONS: These data illustrate that stressor exposure can affect microbial populations, including the lactobacilli, that are closely associated with the colonic mucosa. Because the lactobacilli can have beneficial effects on human health, stressor-induced reductions of their population could have important health implications. BioMed Central 2014-07-15 /pmc/articles/PMC4105248/ /pubmed/25028050 http://dx.doi.org/10.1186/1471-2180-14-189 Text en Copyright © 2014 Galley et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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 Article
Galley, Jeffrey D
Nelson, Michael C
Yu, Zhongtang
Dowd, Scot E
Walter, Jens
Kumar, Purnima S
Lyte, Mark
Bailey, Michael T
Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title_full Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title_fullStr Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title_full_unstemmed Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title_short Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
title_sort exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4105248/
https://www.ncbi.nlm.nih.gov/pubmed/25028050
http://dx.doi.org/10.1186/1471-2180-14-189
work_keys_str_mv AT galleyjeffreyd exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT nelsonmichaelc exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT yuzhongtang exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT dowdscote exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT walterjens exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT kumarpurnimas exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT lytemark exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota
AT baileymichaelt exposuretoasocialstressordisruptsthecommunitystructureofthecolonicmucosaassociatedmicrobiota