Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria

Animals live together with diverse bacteria that can impact their biology. In Drosophila melanogaster, gut-associated bacterial communities are relatively simple in composition but also have a strong impact on host development and physiology. However, it is still unknown if bacteria can proliferate and stably associate with the gut of D. melanogaster. In fact, it is generally assumed that bacteria are transient and their constant ingestion with food is required to maintain their presence in the gut. Here, we identify bacterial species from wild-caught D. melanogaster that stably associate with the host independently of continuous inoculation. Moreover, we show that specific Acetobacter wild isolates can proliferate in the gut. We further demonstrate that the interaction between D. melanogaster and the wild isolated Acetobacter thailandicus is mutually beneficial and that the stability of the gut association is key to this mutualism. The stable population in the gut of D. melanogaster allows continuous bacterial spreading into the environment, which is advantageous to the bacterium itself. The bacterial dissemination is in turn advantageous to the host since the next generation of flies develops in the presence of this particularly beneficial bacterium. Ac. thailandicus leads to a faster host development and higher fertility of emerging adults, when compared to other bacteria isolated from wild-caught flies. Furthermore, Ac. thailandicus is sufficient and advantageous when D. melanogaster develops in axenic or freshly collected figs, respectively. This isolate of Ac. thailandicus colonizes several genotypes of D. melanogaster but not of the closely related Drosophila simulans, indicating that the stable association is host specific. This work establishes a new conceptual model to understand D. melanogaster- gut microbiota interactions in an ecological context; stable interactions can be mutualistic through microbial farming, a common strategy in insects. Moreover, these results develop the use of D. melanogaster as a model to study gut microbiota proliferation and colonization. Author summary Animals, including humans, live together with complex bacterial communities in their gut that influence their physiology and health. The fruit fly Drosophila melanogaster has been an excellent model organism to study host-microbe interactions and harbours a relative simple gut bacterial community. However, it is not known which of these bacteria can proliferate and form stable communities in the gut, and the current hypothesis is that these bacteria are only transiently associated with the gut. Here, we show that in D. melanogaster collected from a natural population stable gut bacteria do exist. We isolated specific species that can proliferate in the gut and form a stable association. This is beneficial to the bacteria since they can be constantly spread by the flies as they move around. On the other hand, this is a form of farming as the next generation of flies benefit from the association with these particular bacteria during development. They become adults faster and are more fertile than if they develop with other bacteria encountered in nature. These advantages are also observed when flies develop in figs, a natural food source. Our findings show that D. melanogaster has stable colonizing bacteria in the gut and establish a new framework to study host-gut bacteria interactions.