Ecological processes underlying bacterial coexistence in the gut are not well understood. Here, we disentangled the effect of the host and the diet on the coexistence of four closely related Lactobacillus species colonizing the honey bee gut. We serially passaged the four species through gnotobiotic bees and in liquid cultures in the presence of either pollen (bee diet) or simple sugars. Although the four species engaged in negative interactions, they were able to stably coexist, both in vivo and in vitro. However, coexistence was only possible in the presence of pollen, and not in simple sugars, independent of the environment. Using metatranscriptomics and metabolomics, we found that the four species utilize different pollen-derived carbohydrate substrates indicating resource partitioning as the basis of coexistence. Our results show that despite longstanding host association, gut bacterial interactions can be recapitulated in vitro providing insights about bacterial coexistence when combined with in vivo experiments.

Ecological processes underlying bacterial coexistence in the gut are not well understood. Here, we disentangled the effect of the host and the diet on the coexistence of four closely related Lactobacillus species colonizing the honey bee gut. We serially passaged the four species through gnotobiotic bees and in liquid cultures in the presence of either pollen (bee diet) or simple sugars. Although the four species engaged in negative interactions, they were able to stably coexist, both in vivo and in vitro. However, coexistence was only possible in the presence of pollen, but not in simple sugars independent of the environment. Using metatranscriptomics and metabolomics, we found that the four species utilize different pollen-derived carbohydrate substrates indicating resource partitioning as the basis of coexistence. Our results show that despite longstanding symbiotic associations, gut bacterial interactions can be recapitulated in vitro providing insights about bacterial coexistence when combined with in vivo experiments.

Nutrients from the host diet and microbial cross-feeding allow diverse bacteria to colonize the animal gut. Less is known about the role of host-derived nutrients in enabling gut bacterial colonization. We examined metabolic interactions within the evolutionary ancient symbiosis between the honey bee (Apis mellifera) and the core gut microbiota memberSnodgrassella alvi. This Betaproteobacteria is incapable of metabolizing saccharides, yet colonizes the honey bee gut in the presence of only a sugar diet. Using comparative metabolomics,13C tracers, and Nanoscale secondary ion mass spectrometry (NanoSIMS), we showin vivothatS. alvigrows on host-derived organic acids, including citrate, glycerate and 3-hydroxy-3-methylglutarate which are actively secreted by the host into the gut lumen.S. alviadditionally modulates tryptophan metabolism in the gut, primarily by converting kynurenine to anthranilate. These results suggest thatSnodgrassellais adapted to a specific metabolic niche in the gut that depends on host-derived nutritional resources.

The composition of the gut microbiota has recently been identified as a cause of cognitive variability in humans and animals. Germ-free individuals and individuals exposed to an antibiotic treatment show severe alteration of their learning and memory performance measured in various cognitive tasks. While different species of bacteria are known to interact in the gut, their cumulative or synergistic effects on cognitive performance remain elusive. Here we established a defined bacterial community - composed of core members of the corbiculate bee microbiota - which enhances honey bee cognitive capacities. Honey bees colonized with this reconstituted community discriminated better two odours based on the presence or absence of a sucrose reward compared to germ-free individuals. They also memorized better these odour-food associations in the short-term. These cognitive improvements seem to constitute an emergent property of the community, because they could not be recapitulated by any of the community member when mono-associated in gnotobiotic bees and they were not explained by the total biomass in the gut. The identification of this community and its effect on bees open new avenues of research in neuroscience, microbiology, and ecology. Future research should help understanding how interactions between bacterial species in the community promote the host associative learning and memory performance.

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