BACKGROUND: Animals form complex symbiotic associations with their gut microbes, whose evolution is determined by an intricate network of host and environmental factors. In many insects, such as Drosophila melanogaster, the microbiome is flexible, environmentally determined, and less diverse than in mammals. In contrast, mammals maintain complex multispecies consortia that are able to colonize and persist in the gastrointestinal tract. Understanding the evolutionary and ecological dynamics of gut microbes in different hosts is challenging. This requires disentangling the ecological factors of selection, determining the timescales over which evolution occurs, and elucidating the architecture of such evolutionary patterns. RESULTS: We employ experimental evolution to track the pace of the evolution of a common gut commensal, Lactiplantibacillus plantarum, within invertebrate (Drosophila melanogaster) and vertebrate (Mus musculus) hosts and their respective diets. We show that in Drosophila, the nutritional environment dictates microbial evolution, while the host benefits L. plantarum growth only over short ecological timescales. By contrast, in a mammalian animal model, L. plantarum evolution results to be divergent between the host intestine and its diet, both phenotypically (i.e., host-evolved populations show higher adaptation to the host intestinal environment) and genomically. Here, both the emergence of hypermutators and the high persistence of mutated genes within the host's environment strongly differed from the low variation observed in the host's nutritional environment alone. CONCLUSIONS: Our results demonstrate that L. plantarum evolution diverges between insects and mammals. While the symbiosis between Drosophila and L. plantarum is mainly determined by the host diet, in mammals, the host and its intrinsic factors play a critical role in selection and influence both the phenotypic and genomic evolution of its gut microbes, as well as the outcome of their symbiosis.

• Keywords
• Drosophila melanogaster, Experimental evolution, Gut microbiota evolution, Host–microbe symbiosis, Lactiplantibacillus plantarum, Mouse, Whole genome sequencing,
• MeSH
• Drosophila melanogaster genetics   MeSH
• Drosophila MeSH
• Microbiota * MeSH
• Mice MeSH
• Mammals MeSH
• Gastrointestinal Microbiome * MeSH
• Symbiosis MeSH
• Animals MeSH
• Check Tag
• Mice MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH

In a single human gut, which is estimated to produce 1000-times more bacteria in a single day than the entire human population on Earth as of 2020, the potential for evolution is vast. In addition to the sheer volume of reproductive events, prokaryotes can transfer most genes horizontally, greatly accelerating their potential to evolve. In the face of this evolutionary potential, Westernization has led to profound changes in the ecosystem of the gut, including increased chronic inflammation in many individuals and dramatically reduced fiber consumption and decreased seasonal variation in the diet of most individuals. Experimental work using a variety of model systems has shown that bacteria will evolve within days to weeks when faced with substantial environmental changes. However, studies evaluating the effects of inflammation of the gut on the microbiota are still in their infancy and generally confounded by the effects of the microbiota on the immune system. At the same time, experimental data indicate that complete loss of fiber from the diet constitutes an extinction-level event for the gut microbiota. However, these studies evaluating diet may not apply to Westernized humans who typically have reduced but not absent levels of fiber in their diet. Thus, while it is expected that the microbiota will evolve rapidly in the face of Westernization, experimental studies that address the magnitude of that evolution are generally lacking, and it remains unknown to what extent this evolutionary process affects disease and the ability to treat the disease state.

• Keywords
• Environment, Evolution, Fiber, Inflammation, Microbiota,
• Publication type
• Journal Article MeSH
• Review MeSH

The Oligo-Mouse-Microbiota (OMM12) is a recently developed synthetic bacterial community for functional microbiome research in mouse models (Brugiroux et al., 2016). To date, the OMM12 model has been established in several germ-free mouse facilities world-wide and is employed to address a growing variety of research questions related to infection biology, mucosal immunology, microbial ecology and host-microbiome metabolic cross-talk. The OMM12 consists of 12 sequenced and publically available strains isolated from mice, representing five bacterial phyla that are naturally abundant in the murine gastrointestinal tract (Lagkouvardos et al., 2016). Under germ-free conditions, the OMM12 colonizes mice stably over multiple generations. Here, we investigated whether stably colonized OMM12 mouse lines could be reproducibly established in different animal facilities. Germ-free C57Bl/6J mice were inoculated with a frozen mixture of the OMM12 strains. Within 2 weeks after application, the OMM12 community reached the same stable composition in all facilities, as determined by fecal microbiome analysis. We show that a second application of the OMM12 strains after 72 h leads to a more stable community composition than a single application. The availability of such protocols for reliable de novo generation of gnotobiotic rodents will certainly contribute to increasing experimental reproducibility in biomedical research.

• Keywords
• 3R, Oligo-MM12, defined bacterial consortia, gnotobiology, isobiotic mice, minimal microbiome, sDMDMm2, syncom,
• Publication type
• Journal Article MeSH