Bacteria from Diverse Habitats Colonize and Compete in the Mouse Gut

Abstract

SUMMARY To study how microbes establish themselves in a mammalian gut environment, we colonized germ-free mice with microbial communities from human, zebrafish and termite guts, human skin and tongue, soil, and estuarine microbial mats. Bacteria from these foreign environments colonized and persisted in the mouse gut; their capacity to metabolize dietary and host carbohydrates, and bile acids, correlated with colonization success. Co-housing mice harboring these xenomicrobiota with one another, with mice harboring native gut microbiota, and germ-free ‘bystanders’ revealed the success of particular bacterial taxa in colonizing an empty gut habitat and guts with established communities. Unanticipated patterns of ecological succession were observed; for example, a soil-derived bacterium dominated even in the presence of bacteria from other gut communities (zebrafish and termite), and human-derived bacteria colonized germ-free mice before mouse-derived organisms. This approach generalizes to address a variety of mechanistic questions about succession, including succession in the context of microbiota-directed therapeutics.

The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota

“…Detailed characterization revealed that 'Flintibacter butyricus' can grow on the amino acids glutamine and glutamate (but not leucine, asparagine, lysine, arginine and aspartic acid), producing up to 7 mM butyrate from 20 mM substrate. Moreover, miBC provides the first cultivable member of the 'Muribaculaceae' (family S24-7), which is known to be a dominant bacterial group in the mouse gut 6 . To confirm the latter observation and assess the occurrence of all novel bacteria within miBC, draft genomes were compared to metagenomic species (MGS) 24 from a comprehensive shotgun sequencing study of the mouse gut metagenome 3 .…”

“…Improving the availability of representative isolates from the mouse gut microbiome is essential for future studies using gnotobiotic mice, particularly because the first reference gene catalogue of the mouse gut microbiota shows very limited overlap with human gut microbial gene diversity 3 . Furthermore, the host species from which bacteria originate influences colonization processes and the effects on host physiology [4][5][6] . Hence, concerted actions to archive and describe bacterial isolates in a host-specific fashion together with appropriate genomic databases are urgently needed 7,8 .…”

Autophagy Protects against Colitis by the Maintenance of Normal Gut Microflora and Secretion of Mucus

“…Therefore, the abnormal microbiota that caused severe colitis in the Atg7 cKO mice may have different properties than the microbiota that were found in previous studies. Seedorf et al (61) reported that bacteria from diverse habitats can colonize in the germfree mouse gut after cohousing. However, in that report, several bacterial groups, such as the soil-derived bacteria, dominated even in the presence of other bacterial communities, whereas some other bacteria could not be easily transmitted from one animal to another animal with an established bacterial community.…”

Evolution of host specialization in gut microbes: the bee gut as a model

“…For specialization, a host-microbe pair should display a direct preferential relationship in addition to any phylogenetic correlation. Perhaps the most straightforward method of testing this is through transplantation experiments, whereby cultured strains (or entire gut communities 21 ) are introduced into gnotobiotic animals, and the microbial colonization load recorded as a proxy for host-microbe compatibility.…”

“…In a competition between a specialized community and an artificially introduced one, however, the one that has evolved to thrive in the gut of that particular host species will almost invariably win out. 21 There are myriad reasons why we should care about host specialization. From a practical standpoint, specialized gut communities are indicative of intimate, evolved interactions between host and microbe, and hence are key to mediating symbiotic benefits that affect host biology.…”