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Mining genome traits that determine the different gut colonization potential of Lactobacillus and Bifidobacterium species.

ABSTRACT: Although the beneficial effects of probiotics are likely to be associated with their ability to colonize the gut, little is known about the characteristics of good colonizers. In a systematic analysis of the comparative genomics, we tried to elucidate the genomic contents that account for the distinct host adaptability patterns of Lactobacillus and Bifidobacterium species. The Bifidobacterium species, with species-level phylogenetic structures affected by recombination among strains, broad mucin-foraging activity, and dietary-fibre-degrading ability, represented niche conservatism and tended to be host-adapted. The Lactobacillus species stretched across three lifestyles, namely free-living, nomadic and host-adapted, as characterized by the variations of bacterial occurrence time, guanine-cytosine (GC) content and genome size, evolution event frequency, and the presence of human-adapted bacterial genes. The numbers and activity of host-adapted factors, such as bile salt hydrolase and intestinal tissue-anchored elements, were distinctly distributed among the three lifestyles. The strains of the three lifestyles could be separated with such a collection of colonization-related genomic content (genes, genome size and GC content). Thus, our work provided valuable information for rational selection and gut engraftment prediction of probiotics. Here, we have found many interesting predictive results for bacterial gut fitness, which will be validated in vitro and in vivo.

SUBMITTER: Xiao Y

PROVIDER: S-EPMC8461469 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:The microbiota presents a compartmentalized distribution across different gut segments. Hence, the exogenous microbiota from a particular gut segment might only invade its homologous gut location during microbiota transplantation. Feces as the excreted residue contain most of the large-intestinal microbes but lack small-intestinal microbes. We speculated that whole-intestinal microbiota transplantation (WIMT), comprising jejunal, ileal, cecal, and colonic microbiota, would be more effective for reshaping the entire intestinal microbiota than conventional fecal microbiota transplantation fecal microbiota transplantation (FMT). RESULTS:We modeled the compartmentalized colonization of the gut microbiota via transplanting the microbiota from jejunum, ileum, cecum, and colon, respectively, into the germ-free mice. Transplanting jejunal or ileal microbiota induced more exogenous microbes' colonization in the small intestine (SI) of germ-free mice rather than the large intestine (LI), primarily containing Proteobacteria, Lactobacillaceae, and Cyanobacteria. Conversely, more saccharolytic anaerobes from exogenous cecal or colonic microbiota, such as Bacteroidetes, Prevotellaceae, Lachnospiraceae, and Ruminococcaceae, established in the LI of germ-free mice that received corresponding intestinal segmented microbiota transplantation. Consistent compartmentalized colonization patterns of microbial functions in the intestine of germ-free mice were also observed. Genes related to nucleotide metabolism, genetic information processing, and replication and repair were primarily enriched in small-intestinal communities, whereas genes associated with the metabolism of essential nutrients such as carbohydrates, amino acids, cofactors, and vitamins were mainly enriched in large-intestinal communities of germ-free mice. Subsequently, we compared the difference in reshaping the community structure of germ-free mice between FMT and WIMT. FMT mainly transferred LI-derived microorganisms and gene functions into the recipient intestine with sparse SI-derived microbes successfully transplanted. However, WIMT introduced more SI-derived microbes and associated microbial functions to the recipient intestine than FMT. Besides, WIMT also improved intestinal morphological development as well as reduced systematic inflammation responses of recipients compared with FMT. CONCLUSIONS:Segmented exogenous microbiota transplantation proved the spatial heterogeneity of bacterial colonization along the gastrointestinal tract, i.e., the microbiota from one specific location selectively colonizes its homologous gut region. Given the lack of exogenous small-intestinal microbes during FMT, WIMT may be a promising alternative for conventional FMT to reconstitute the microbiota across the entire intestinal tract. Video Abstract.

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Mining genome traits that determine the different gut colonization potential of Lactobacillus and Bifidobacterium species.

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