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. It is generally assumed that gut bacteria in D. melanogaster 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 because the next generation of flies develops in the presence of this particularly beneficial bacterium. A. thailandicus leads to a faster host development and higher fertility of emerging adults when compared to other bacteria isolated from wild-caught flies. Furthermore, A. thailandicus is sufficient and advantageous when D. melanogaster develops in axenic or freshly collected figs, respectively. This isolate of A. thailandicus colonizes several genotypes of D. melanogaster but not the closely related D. 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.

动物与多种可影响其生物学特性的细菌共生。在黑腹果蝇（Drosophila melanogaster）中，肠道相关细菌群落的组成相对简单，但却对宿主的发育与生理机能具有显著影响。学界普遍认为，黑腹果蝇的肠道细菌为暂时性菌群，且需通过持续随食物摄入才能维持其在肠道内的存在。本研究中，我们从野外捕获的黑腹果蝇中分离出可独立于持续接种而与宿主稳定共生的细菌物种。此外，我们证实特定的野生醋杆菌（Acetobacter）分离株可在肠道内增殖。我们进一步证实，黑腹果蝇与野生分离得到的泰国醋杆菌（Acetobacter thailandicus）之间的相互作用为互利共生，而肠道共生的稳定性是该共生关系的核心。黑腹果蝇肠道内的稳定菌群可使细菌持续扩散至环境中，这对细菌自身极为有利。而细菌的传播反过来也有益于宿主，因为果蝇的下一代将在这种极具益生性的细菌存在的环境中发育。相较于其他从野生果蝇中分离的细菌，泰国醋杆菌可加快宿主发育速度，并提高羽化成虫的繁殖力。此外，当黑腹果蝇分别在无菌环境或新鲜采集的无花果中发育时，泰国醋杆菌即可发挥充足且有益的作用。该泰国醋杆菌分离株可定植于多种基因型的黑腹果蝇体内，但无法定植亲缘关系相近的拟果蝇（Drosophila simulans），这表明这种稳定共生具有宿主特异性。本研究构建了一种全新的概念模型，用于在生态学背景下解析黑腹果蝇与肠道菌群的相互作用；稳定的共生关系可通过微生物耕作这一昆虫常见生存策略实现互利共生。此外，本研究结果还拓展了黑腹果蝇作为研究肠道菌群增殖与定植模型的应用范围。