Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community

Abstract

Microbe-microbe interactions are critical for gut microbiome function. A challenging task to understand health and disease-related microbiome signatures is to move beyond descriptive community-level profiling towards disentangling microbial interaction networks. Here, we aimed to determine members taking on a keystone role in shaping community ecology of a widely used synthetic bacterial community (OMM12). Using single-species dropout communities and metabolomic profiling, we identified Bacteroides caecimuris I48, Blautia coccoides YL58 and Enterococcus faecalis KB1 as major drivers of in vitro community assembly and elucidated underlying mechanisms of these keystone functions. Importantly, keystone species and bacterial strain relationships were found to strongly vary across different nutritional conditions, depending on the strains' potential to modify the corresponding environment. Further, gnotobiotic mice transplanted with communities lacking B. caecimuris I48 and B. coccoides YL58 exhibited morphological anomalies and altered intestinal metabolomic profiles, exposing physiologically relevant functions of these keystone community members. In summary, the presented study experimentally confirms the strong interdependency between bacterial community ecology and the biotic and abiotic environment, underlining the context-dependency and conditionality of bacterial interaction networks.

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“…Also the transfer of potentially beneficial metabolic genes from temperate phages to their bacterial hosts [88][89][90][91] , may enhance host competitiveness and contribute to overall GM changes. These findings align with recent research demonstrating how metabolic functions and bacterial interaction networks were context-dependent of variables like nutrition, host environment, and bacterial compositions 92 , supporting the hypothesis that cascading events initiated by FVT could catalyze GM modulating effects. In addition to the bacteria-phage relations, the impact of the immune system on gut health should not be neglected.…”

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“…Furthermore, the transfer of potentially beneficial metabolic genes from temperate phages to their bacterial hosts may enhance host competitiveness and contribute to overall microbiota changes [92,93]. These findings align with recent research demonstrating the significant influence of nutritional and host environments on the community ecology [94], suggesting that cascading events initiated by FVT could catalyze changes in the host environment. Beyond the bacteria-phage relations, the role of the immune system in gut health should not be underestimated.…”

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“…Overall, this suggests that the interactions identified between the cirrhotic species are context-dependent, a finding that has already been documented in other contexts Weiss et al [2023] and K. Faust [2021].…”