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Comparing the gut microbiome along the gastrointestinal tract of three sympatric species of wild rodents.

ABSTRACT: Host-microbe interactions within the gastrointestinal tract (GIT) play a pivotal role in shaping host physiology, ecology, and life history. However, these interactions vary across gut regions due to changes in the physical environment or host immune system activity, thereby altering the microbial community. Each animal species may harbor their own unique microbial community due to host species-specific ecological traits such as dietary habits, micro-habitat preferences, and mating behavior as well as physiological traits. While the gut microbiota in wild animals has received much attention over the last decade, most studies comparing closely related species only utilized fecal or colon samples. In this study, we first compared the gut microbial community from the small intestine, cecum, colon, and rectum within three sympatric species of wild rodents (i.e. Apodemus speciosus, A. argenteus, and Myodes rufocanus). We then compared each gut region among host species to determine the effect of both gut region and host species on the gut microbiota. We found that the small intestine harbored a unique microbiome as compared to the lower GIT in all three host species, with the genus Lactobacillus in particular having higher abundance in the small intestine of all three host species. There were clear interspecific differences in the microbiome within all gut regions, although some similarity in alpha diversity and community structure within the small intestine was found. Finally, fecal samples may be appropriate for studying the lower GIT in these species, but not the small intestine.

SUBMITTER: Anders JL

PROVIDER: S-EPMC8497572 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe proliferation and survival of microbial organisms including intestinal microbes are determined by their surrounding environments. Contrary to popular myth, the nutritional and chemical compositions, water contents, O2 contents, temperatures, and pH in the gastrointestinal (GI) tract of a human are very different in a location-specific manner, implying heterogeneity of the microbial composition in a location-specific manner.ResultsWe first investigated the environmental conditions at 6 different locations along the GI tract and feces of ten weeks' old male SPF C57BL/6 mice. As previously known, the pH and water contents of the GI contents at the different locations of the GI tract were very different from each other in a location-specific manner, and none of which were not even similar to those of feces. After confirming the heterogeneous nature of the GI contents in specific locations and feces, we thoroughly analyzed the composition of the microbiome of the GI contents and feces. 16S rDNA-based metagenome sequencing on the GI contents and feces showed the presence of 13 different phyla. The abundance of Firmicutes gradually decreased from the stomach to feces while the abundance of Bacteroidetes gradually increased. The taxonomic α-diversities measured by ACE (Abundance-based Coverage Estimator) richness, Shannon diversity, and Fisher's alpha all indicated that the diversities of gut microbiome at colon and cecum were much higher than that of feces. The diversities of microbiome compositions were lowest in jejunum and ileum while highest in cecum and colon. Interestingly, the diversities of the fecal microbiome were lower than those of the cecum and colon. Beta diversity analyses by NMDS plots, PCA, and unsupervised hierarchical clustering all showed that the microbiome compositions were very diverse in a location-specific manner. Direct comparison of the fecal microbiome with the microbiome of the whole GI tracts by α-and β-diversities showed that the fecal microbiome did not represent the microbiome of the whole GI tract.ConclusionThe fecal microbiome is different from the whole microbiome of the GI tract, contrary to a baseline assumption of contemporary microbiome research work.

Project description:Intestinal efflux transporters affect the gastrointestinal processing of many drugs but further data on their intestinal expression levels are required. Relative mRNA expression and relative and absolute protein expression data of transporters are commonly measured by real-time polymerase chain reaction (RT-PCR), Western blot and mass spectrometry-based targeted proteomics techniques. All of these methods, however, have their own strengths and limitations, and therefore, validation for optimized quantification methods is needed. As such, the identification of the most appropriate technique is necessary to effectively translate preclinical findings to first-in-human trials. In this study, the mRNA expression and protein levels of the efflux transporter P-glycoprotein (P-gp) in jejunal and ileal epithelia of 30 male and female human subjects, and the duodenal, jejunal, ileal and colonic tissues in 48 Wistar rats were quantified using RT-PCR, Western blot and liquid chromatography-tandem mass spectrometry (LC-MS/MS). A similar sex difference was observed in the expression of small intestinal P-gp in humans and Wistar rats where P-gp was higher in males than females with an increasing trend from the proximal to the distal parts in both species. A strong positive linear correlation was determined between the Western blot data and LC-MS/MS data in the small intestine of humans (R2 = 0.85). Conflicting results, however, were shown in rat small intestinal and colonic P-gp expression between the techniques (R2 = 0.29 and 0.05, respectively). In RT-PCR and Western blot, an internal reference protein is experimentally required; here, beta-actin was used which is innately variable along the intestinal tract. Quantification via LC-MS/MS can provide data on P-gp expression without the need for an internal reference protein and consequently, can give higher confidence on the expression levels of P-gp along the intestinal tract. Overall, these findings highlight similar trends between the species and suggest that the Wistar rat is an appropriate preclinical animal model to predict the oral drug absorption of P-gp substrates in the human small intestine.

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Comparing the gut microbiome along the gastrointestinal tract of three sympatric species of wild rodents.

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