Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota - PubMed (original) (raw)

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

Jeffrey D Galley et al. BMC Microbiol. 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.

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Figures

Figure 1

Figure 1

Exposure to the SDR stressor did not impact alpha-diversity. Mice were exposed to the SDR stressor, or were left undisturbed as non-stressed Home Cage controls (HCC control). After 454 pyrosequencing, three measures of community alpha-diversity were calculated using QIIME. A. Equitability Index, B. Shannon Diversity Index, and C. Chao1 Rarefaction Measurement were unaffected by exposure to the SDR stressor. Data are from n = 5 mice per group.

Figure 2

Figure 2

Exposure to the SDR stressor significantly changes beta-diversity. After 454 pyrosequencing, UniFrac distances were calculated using QIIME and plotted on a 2-D principal coordinates graph (A). Exposure to the SDR stressor shifted the colonic microbiota, with 4 of 5 SDR stressor samples clustering apart from HCC controls. UniFrac distances were also used for construction of an unweighted pair group method by arithmetic mean (UPGMA) dendrogram, in which 4 of 5 SDR stressor samples clustered together (B). The clustering in Figure 2A and 2B was statistically significant (p < 0.05) after performing the ANOSIM test to measure differences between distance matrices of SDR stressor and HCC control groups. Data are from n = 5 mice per group.

Figure 3

Figure 3

The relative abundances of mucosal-associated bacterial phyla were unaffected by exposure to the SDR stressor. Data are the mean+/-S.E. of the relative abundances calculated from 454 pyrosequencing data and are from n = 5 mice per group.

Figure 4

Figure 4

The absolute abundance of bacteria in the genus Lactobacillus is reduced by exposure to the SDR stressor. Mice were exposed to either 0, 1, or 6 consecutive days of the SDR stressor and qPCR used to quantify Lactobacillus group bacteria (A and B) or L. reuteri (C) in the colon. *indicates p < .05 vs. 0 cycles of SDR (0 cycles is equivalent to HCC controls). Inbred C57Bl/6- n = 16 at Day 0, n = 7 on Day 1, and n = 8 on Day 6. Outbred CD-1- n = 21 at Day 0, n = 15 at Day 1, and n = 6 on Day 6.

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