<i>Drosophila melanogaster</i> establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria

<div><p>Animals live together with diverse bacteria that can impact their biology. In <i>Drosophila melanogaster</i>, gut-associated bacterial communities are relatively simple in composition but also have a strong impact on host development and physiology. It is generally assumed that gut bacteria in <i>D</i>. <i>melanogaster</i> 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 <i>D</i>. <i>melanogaster</i> that stably associate with the host independently of continuous inoculation. Moreover, we show that specific <i>Acetobacter</i> wild isolates can proliferate in the gut. We further demonstrate that the interaction between <i>D</i>. <i>melanogaster</i> and the wild isolated <i>Acetobacter thailandicus</i> is mutually beneficial and that the stability of the gut association is key to this mutualism. The stable population in the gut of <i>D</i>. <i>melanogaster</i> allows continuous bacterial spreading into the environment, which is advantageous to the bacterium itself. The bacterial dissemination is in turn advantageous to the host because the next generation of flies develops in the presence of this particularly beneficial bacterium. <i>A</i>. <i>thailandicus</i> leads to a faster host development and higher fertility of emerging adults when compared to other bacteria isolated from wild-caught flies. Furthermore, <i>A</i>. <i>thailandicus</i> is sufficient and advantageous when <i>D</i>. <i>melanogaster</i> develops in axenic or freshly collected figs, respectively. This isolate of <i>A</i>. <i>thailandicus</i> colonizes several genotypes of <i>D</i>. <i>melanogaster</i> but not the closely related <i>D</i>. <i>simulans</i>, indicating that the stable association is host specific. This work establishes a new conceptual model to understand <i>D</i>. <i>melanogaster</i>–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 <i>D</i>. <i>melanogaster</i> as a model to study gut microbiota proliferation and colonization.</p>