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Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.

ABSTRACT: The bodies of most animals are populated by highly complex and genetically diverse communities of microorganisms. The majority of these microbes reside within the intestines in largely stable but dynamically interactive climax communities that positively interact with their host. Studies from this laboratory have shown that stressor exposure impacts the stability of the microbiota and leads to bacterial translocation. The biological importance of these alterations, however, is not well understood. To determine whether the microbiome contributes to stressor-induced immunoenhancement, mice were exposed to a social stressor called social disruption (SDR), that increases circulating cytokines and primes the innate immune system for enhanced reactivity. Bacterial populations in the cecum were characterized using bacterial tag-encoded FLX amplicon pyrosequencing. Stressor exposure significantly changed the community structure of the microbiota, particularly when the microbiota were assessed immediately after stressor exposure. Most notably, stressor exposure decreased the relative abundance of bacteria in the genus Bacteroides, while increasing the relative abundance of bacteria in the genus Clostridium. The stressor also increased circulating levels of IL-6 and MCP-1, which were significantly correlated with stressor-induced changes to three bacterial genera (i.e., Coprococcus, Pseudobutyrivibrio, and Dorea). In follow up experiments, mice were treated with an antibiotic cocktail to determine whether reducing the microbiota would abrogate the stressor-induced increases in circulating cytokines. Exposure to SDR failed to increase IL-6 and MCP-1 in the antibiotic treated mice. These data show that exposure to SDR significantly affects bacterial populations in the intestines, and remarkably also suggest that the microbiota are necessary for stressor-induced increases in circulating cytokines.

SUBMITTER: Bailey MT

PROVIDER: S-EPMC3039072 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.

Bailey Michael T MT Dowd Scot E SE Galley Jeffrey D JD Hufnagle Amy R AR Allen Rebecca G RG Lyte Mark M

Brain, behavior, and immunity 20101030 3

The bodies of most animals are populated by highly complex and genetically diverse communities of microorganisms. The majority of these microbes reside within the intestines in largely stable but dynamically interactive climax communities that positively interact with their host. Studies from this laboratory have shown that stressor exposure impacts the stability of the microbiota and leads to bacterial translocation. The biological importance of these alterations, however, is not well understoo ...[more]

PMID: 21040780

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Project description: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.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.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.

Project description:The gut microbiome is a complex ecosystem that contributes to host nutrition and health. However, our current knowledge of the relationship between ambient temperature and gut microbiota of poultry is still limited. The objective of the present study was to characterize the intestinal microbiota of ducks exposed to high ambient temperature. Sixty 60-day-old Shaoxing ducks were allocated to control and heat-treated groups. The ducks in the control group were kept at 25°C, and the ducks in the heat treatment group were raised at 30-40°C, which simulated the temperature change of day and night in summer. After 15 D, the intestinal contents of the duodenum, jejunum, and ileum were obtained from 6 ducks of each group. Genomic DNA was extracted and amplified based on the V4-V5 hypervariable region of 16S rRNA. The results showed that Firmicutes was the dominant bacterial phylum with the highest abundance in the contents of the small intestine of ducks, and the relative abundance of the phylum Firmicutes in all 3 intestinal segments was increased by high temperature. At the genus level, Lactobacillus was found to be the most dominant bacterial genus across 3 gut segments, and its abundance was increased in ducks under heat treatment. Compared with the corresponding intestine segment of control ducks, a total of 36 genera in the duodenum, 19 genera in the jejunum, and 6 genera in the ileum of heat-treated ducks were found to be significantly different in the abundance (linear discriminant analysis score >3.0, P < 0.05). Functional prediction of gut microbiota revealed that high temperature caused changes in the abundance of metabolism and transcription-related pathways. It is noteworthy that most of the altered pathways are related to metabolism. In conclusion, high temperature induced remarkable taxonomic changes in the gut microbiome of ducks, which might be related to the negative effects of high temperature in ducks. Our present study provided an important theoretical ground for high-temperature intervention.

Dataset Information

Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.

Publications

Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.

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