Microbiota plasticity aids invasive fruit fly adaptation to plant secondary metabolites

The gut microbiota of herbivorous insects plays a crucial role in coordinating their hosts' life history and performance in response to the chemical defenses of various plant secondary metabolites (PSMs). We investigated the effects of 11 fruits and PSMs on the pupal weight, survival, and gut microbiota of the invasive fruit fly Bactrocera dorsalis. Our results show that B. dorsalis exhibits notable variation in pupal weight across a wide range of fruits of host plant species. Flies reared conventionally adapted to different PSMs, whereas germ-free flies suffered significant weight loss when exposed to PSMs such as cyanidin, GABA, salicylic acid, and shikimic acid. The gut microbiota of B. dorsalis demonstrated both a resilient core module and a functionally flexible module that responded to PSMs supplementation. Notably, the family Lactobacillaceae exhibited significant malleability, with Companilactobacillus pabuli, Lactiplantibacillus plantarum, and Levilactobacillus brevis mitigating the adverse effects of PSMs on growth, though not on survival. Flies supplemented with multiple Lactobacillaceae species performed better in adapting to PSMs than those supplemented with single species. Genomic analyses of bacterial isolates identified key enzyme genes involved in PSM metabolism, and molecular docking analyses underscored their crucial role in the gut microbiota of B. dorsalis. The plasticity of the gut microbiota modulates host adaptation to PSM defenses by altering microbial functional composition. These findings highlight the role of the gut microbiome in conferring adaptability to PSMs in plant-insect interactions.