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Mucosal Microbiota and Metabolome along the Intestinal Tract Reveal a Location-Specific Relationship.

ABSTRACT: The intestinal microbiota is highly metabolically active and plays an important role in many metabolic processes absent from the human host. Altered microbiota metabolism has been linked to diseases such as obesity, cardiovascular disease, and colorectal cancer. However, there is a gap in the current knowledge on how the microbiota interact with its host in terms of metabolic interactions. Here, we performed an integrated analysis between the mucosa-associated microbiota and the mucosa metabolome in healthy, nonhuman primates to investigate these relationships. The microbiota composition was distinct at each tissue location, with variation by host individual also observed. Microbiota-metabolome dynamics were primarily driven by interactions in the distal colon. These interactions were strongly correlated with dietary component, indicating a possibility to modulate microbiota-metabolomic interactions using prebiotic strategies.IMPORTANCE In a healthy colon, the microbiota produces a vast amount of metabolites that are essential to maintaining homeostasis in the colon microenvironment. In fact, these metabolites produced by the microbiota have been linked to diseases such as obesity, cardiovascular disease, and colorectal cancer. In this study, we used healthy nonhuman primate models to investigate the relationship between microbiota and tissue metabolites. We found that both microbiota and metabolites have location-specific signatures along the intestine. Most importantly, we found that metabolites from food sources correlate with multiple bacteria in different intestinal locations. Overall, this work presents a systems-level map of the association between the microbiota and the metabolites in healthy nonhuman primates, provides candidates for experimental validation, and suggests a possibility to regulate the gut microbiota through specific prebiotic combinations.

SUBMITTER: Yuan C

PROVIDER: S-EPMC7253361 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Mucosal Microbiota and Metabolome along the Intestinal Tract Reveal a Location-Specific Relationship.

Yuan Ce C Graham Melanie M Staley Christopher C Subramanian Subbaya S

mSystems 20200526 3

The intestinal microbiota is highly metabolically active and plays an important role in many metabolic processes absent from the human host. Altered microbiota metabolism has been linked to diseases such as obesity, cardiovascular disease, and colorectal cancer. However, there is a gap in the current knowledge on how the microbiota interact with its host in terms of metabolic interactions. Here, we performed an integrated analysis between the mucosa-associated microbiota and the mucosa metabolom ...[more]

PMID: 32457236

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Project description:To gain insight into the importance of carefully selecting the sampling area for intestinal microbiota studies, cecal and fecal microbial communities of Caldes meat rabbit were characterized. The animals involved in the study were divided in two groups according to the feed intake level they received during the fattening period; ad libitum (n = 10) or restricted to 75% of ad libitum intake (n = 11). Cecum and internal hard feces were sampled from sacrificed animals. Assessment of bacterial and archaeal populations was performed by means of Illumina sequencing of 16S rRNA gene amplicons in a MiSeq platform. A total of 596 operational taxonomic units (OTUs) were detected using QIIME software. Taxonomic assignment revealed that microbial diversity was dominated by phyla Firmicutes (76.42%), Tenericutes (7.83%), and Bacteroidetes (7.42%); kingdom Archaea was presented at low percentage (0.61%). No significant differences were detected between sampling origins in microbial diversity or richness assessed using two alpha-diversity indexes: Shannon and the observed number of OTUs. However, the analysis of variance at genus level revealed a higher presence of genera Clostridium, Anaerofustis, Blautia, Akkermansia, rc4-4, and Bacteroides in cecal samples. By contrast, genera Oscillospira and Coprococcus were found to be overrepresented in feces, suggesting that bacterial species of these genera would act as fermenters at the end of feed digestion process. At the lowest taxonomic level, 83 and 97 OTUs in feces and cecum, respectively, were differentially represented. Multivariate statistical assessment revealed that sparse partial least squares discriminant analysis (sPLS-DA) was the best approach for this purpose. Interestingly, the majority of the most discriminative OTUs selected by sPLS-DA were found to be differentially represented between sampling origins in univariate analysis. Our study provides evidence that the choice of intestinal sampling area is relevant due to important differences in some taxa's relative abundance that have been revealed between rabbits' cecal and fecal microbiota. An appropriate sampling intestinal area should be chosen in each microbiota assessment.

Project description:Background: The farnesoid X receptor (FXR) is a key factor regulating hepatic bile acid synthesis and enterohepatic circulation. Repression of bile acid synthesis by the FXR is a potential strategy for treating cholestatic liver disease. However, the role of intestinal FXR on the intestinal barrier and intestinal microbiota needs further investigation. Materials: Intestinal tissues were collected from patients with biliary atresia or without hepatobiliary disease. Then, intestinal mRNA levels of FXR-related molecules were determined. To investigate the effect of FXR activation, bile-duct-ligation rats were treated with obeticholic acid [OCA (5 mg/kg/day)] or vehicle (0.5% methyl cellulose) per oral gavage for 14 days. The mRNA levels of intestinal FXR, SHP, TNF-α, FGF15 and bile acid transporter levels were determined. In addition, the intestinal permeability, morphologic changes, and composition of the intestinal microbiota were evaluated. Gut Microbiome was determined by 16S rDNA MiSeq sequencing, and functional profiling of microbial communities was predicted with BugBase and PICRUSt2. Finally, the role of OCA in injured intestinal epithelial cell apoptosis and proliferation was examined by pretreatment with lipopolysaccharide (LPS) in Caco-2 cells. Results: The downstream of the FXR in ileum tissues was inhibited in biliary obstruction. Activation of the FXR signaling pathway by OCA significantly reduced liver fibrosis and intestinal inflammation, improved intestinal microbiota, and protected intestinal mucosa in BDL rats. OCA also altered the functional capacities of ileum microbiota in BDL rats. Significant differences existed between the controls and BDL rats, which were attenuated by OCA in the alpha diversity analysis. Principal coordinates analysis showed that microbial communities in BDL rats clustered separately from controls, and OCA treatment attenuated the distinction. Bugbase and PICRUSt2 analysis showed that OCA changed the composition and structure of the intestinal microbiota and improved the metabolic function of the intestinal microbiota by increasing the relative abundance of beneficial bacteria and reducing the relative abundance of harmful bacteria. Moreover, OCA reduced the apoptosis induced by LPS in Caco-2 cells. Conclusion: The FXR agonist, OCA, activates the intestinal FXR signaling pathway and improves the composition and structure of the intestinal microbiota and intestinal barrier in BDL rats.

Dataset Information

Mucosal Microbiota and Metabolome along the Intestinal Tract Reveal a Location-Specific Relationship.

Publications

Mucosal Microbiota and Metabolome along the Intestinal Tract Reveal a Location-Specific Relationship.

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