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Open Access Research article

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

Jeffrey D Galley1, Michael C Nelson2, Zhongtang Yu3, Scot E Dowd4, Jens Walter5, Purnima S Kumar6, Mark Lyte7 and Michael T Bailey189*

Author Affiliations

1 Biosciences Division, College of Dentistry, The Ohio State University, Columbus, USA

2 Department of Molecular and Cell Biology, University of Connecticut, Storrs, USA

3 Department of Animal Sciences, The Ohio State University, Columbus, USA

4 Molecular Research Mr DNA Laboratory, Shallowater, USA

5 Departments of Agricultural, Food & Nutritional Science and of Biological Sciences, University of Alberta, Edmonton, Canada

6 Division of Periodontology, College of Dentistry, The Ohio State University, Columbus, USA

7 Department of Immunotherapeutics and Biotechnology, School of Pharmacy, Texas Tech University Health Sciences Center, Abilene, USA

8 Institute for Behavioral Medicine Research, Wexner Medical Center, The Ohio State University, 329A IBMR Building, 460 Medical Center Dr, Columbus, OH 43210, USA

9 Department of Pediatrics, Wexner Medical Center, The Ohio State University, Columbus, USA

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BMC Microbiology 2014, 14:189  doi:10.1186/1471-2180-14-189

Published: 15 July 2014

Abstract

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.

Keywords:
Psychological stress; Gastrointestinal microbiota; Lactobacillus; Lactobacillus reuteri; Dysbiosis