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Spatial Heterogeneity of Gut Microbial Composition along the Gastrointestinal Tract in Natural Populations of House Mice

View Article: PubMed Central - PubMed

ABSTRACT

There is a growing appreciation of the role of gut microbial communities in host biology. However, the nature of variation in microbial communities among different segments of the gastrointestinal (GI) tract is not well understood. Here, we describe microbial communities from ten different segments of the GI tract (mouth, esophagus, stomach, duodenum, ileum, proximal cecum, distal cecum, colon, rectum, and feces) in wild house mice using 16S rRNA gene amplicon sequencing. We also measured carbon and nitrogen stable isotopic ratios from hair samples of individual mice as a proxy for diet. We identified factors that may explain differences in microbial composition among gut segments, and we tested for differences among individual mice in the composition of the microbiota. Consistent with previous studies, the lower GI tract was characterized by a greater relative abundance of anaerobic bacteria and greater microbial diversity relative to the upper GI tract. The upper and lower GI tracts also differed in the relative abundances of predicted microbial gene functions, including those involved in metabolic pathways. However, when the upper and lower GI tracts were considered separately, gut microbial composition was associated with individual mice. Finally, microbial communities derived from fecal samples were similar to those derived from the lower GI tract of their respective hosts, supporting the utility of fecal sampling for studying the gut microbiota of mice. These results show that while there is substantial heterogeneity among segments of the GI tract, individual hosts play a significant role in structuring microbial communities within particular segments of the GI tract.

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Related in: MedlinePlus

The relative proportions of the most abundant metabolism related KEGG pathways (level 3) predicted by PICRUSt between upper and lower GI tract.The error bars are standard deviations. The star indicates Bonferroni corrected P < 0.0033 using Wilcoxson rank sum test.
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pone.0163720.g002: The relative proportions of the most abundant metabolism related KEGG pathways (level 3) predicted by PICRUSt between upper and lower GI tract.The error bars are standard deviations. The star indicates Bonferroni corrected P < 0.0033 using Wilcoxson rank sum test.

Mentions: The predicted functions of the gut microbial community differed between the upper and lower GI tract. The first principle component of the relative abundances of microbial gene functions (KEGG pathway categories) predicted from the 16S rRNA gene data showed a significant difference between the upper and lower GI tract (Wilcoxon rank sum test P < 0.0001) (Fig 1D). The gene function PC1 was enriched in metabolism functions, where 11 out of the top 15 eigenvectors were categorized to functions related to metabolism (Table G in S1 File). Gene function PC1 significantly differed among the gut segments within the upper GI tract (Kruskal-Wallis test, P = 0.006), but not within the lower GI tract (Kruskal-Wallis test, P = 0.14). The differences among the gut segments in the upper GI tract were not significant after multiple corrections (Wilcoxon rank sum test, Bonferroni corrected P < 0.005). To test whether the abundance of genes in various metabolic pathways differed between the upper and lower GI tract, we focused on the top 15 most abundant metabolism gene function categories. Most of the metabolism gene function categories showed significant differences in their relative abundances between the upper and lower GI tract (Fig 2).


Spatial Heterogeneity of Gut Microbial Composition along the Gastrointestinal Tract in Natural Populations of House Mice
The relative proportions of the most abundant metabolism related KEGG pathways (level 3) predicted by PICRUSt between upper and lower GI tract.The error bars are standard deviations. The star indicates Bonferroni corrected P < 0.0033 using Wilcoxson rank sum test.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5036816&req=5

pone.0163720.g002: The relative proportions of the most abundant metabolism related KEGG pathways (level 3) predicted by PICRUSt between upper and lower GI tract.The error bars are standard deviations. The star indicates Bonferroni corrected P < 0.0033 using Wilcoxson rank sum test.
Mentions: The predicted functions of the gut microbial community differed between the upper and lower GI tract. The first principle component of the relative abundances of microbial gene functions (KEGG pathway categories) predicted from the 16S rRNA gene data showed a significant difference between the upper and lower GI tract (Wilcoxon rank sum test P < 0.0001) (Fig 1D). The gene function PC1 was enriched in metabolism functions, where 11 out of the top 15 eigenvectors were categorized to functions related to metabolism (Table G in S1 File). Gene function PC1 significantly differed among the gut segments within the upper GI tract (Kruskal-Wallis test, P = 0.006), but not within the lower GI tract (Kruskal-Wallis test, P = 0.14). The differences among the gut segments in the upper GI tract were not significant after multiple corrections (Wilcoxon rank sum test, Bonferroni corrected P < 0.005). To test whether the abundance of genes in various metabolic pathways differed between the upper and lower GI tract, we focused on the top 15 most abundant metabolism gene function categories. Most of the metabolism gene function categories showed significant differences in their relative abundances between the upper and lower GI tract (Fig 2).

View Article: PubMed Central - PubMed

ABSTRACT

There is a growing appreciation of the role of gut microbial communities in host biology. However, the nature of variation in microbial communities among different segments of the gastrointestinal (GI) tract is not well understood. Here, we describe microbial communities from ten different segments of the GI tract (mouth, esophagus, stomach, duodenum, ileum, proximal cecum, distal cecum, colon, rectum, and feces) in wild house mice using 16S rRNA gene amplicon sequencing. We also measured carbon and nitrogen stable isotopic ratios from hair samples of individual mice as a proxy for diet. We identified factors that may explain differences in microbial composition among gut segments, and we tested for differences among individual mice in the composition of the microbiota. Consistent with previous studies, the lower GI tract was characterized by a greater relative abundance of anaerobic bacteria and greater microbial diversity relative to the upper GI tract. The upper and lower GI tracts also differed in the relative abundances of predicted microbial gene functions, including those involved in metabolic pathways. However, when the upper and lower GI tracts were considered separately, gut microbial composition was associated with individual mice. Finally, microbial communities derived from fecal samples were similar to those derived from the lower GI tract of their respective hosts, supporting the utility of fecal sampling for studying the gut microbiota of mice. These results show that while there is substantial heterogeneity among segments of the GI tract, individual hosts play a significant role in structuring microbial communities within particular segments of the GI tract.

No MeSH data available.


Related in: MedlinePlus