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.

植食性昆虫的肠道菌群在协调宿主生活史与生存表现、应对多种植物次生代谢物（Plant Secondary Metabolites，简称PSMs）的化学防御方面发挥着关键作用。本研究探究了11种果实及PSMs对入侵性实蝇橘小实蝇（*Bactrocera dorsalis*）的蛹重、存活率及肠道菌群的影响。研究结果显示，取食多种寄主植物果实的橘小实蝇，其蛹重存在显著差异。常规饲养的实蝇能够适应不同的PSMs，而无菌实蝇在接触矢车菊素、γ-氨基丁酸（GABA）、水杨酸以及莽草酸等PSMs时，会出现显著的体重下降。橘小实蝇的肠道菌群同时具备抗性核心模块与功能柔性模块，可响应PSMs的添加处理。值得注意的是，乳杆菌科（Lactobacillaceae）展现出显著的可塑性：帕布伴乳杆菌（*Companilactobacillus pabuli*）、植物乳杆菌（*Lactiplantibacillus plantarum*）以及短乳杆菌（*Levilactobacillus brevis*）可缓解PSMs对实蝇生长的不利影响，但对存活率无显著作用。同时添加多种乳杆菌科菌株的实蝇，在适应PSMs方面的表现优于仅添加单一菌株的实蝇。对分离菌株的基因组分析鉴定出参与PSMs代谢的关键酶基因，分子对接分析则进一步证实了这些基因在橘小实蝇肠道菌群中的核心作用。肠道菌群的可塑性可通过改变微生物的功能组成，调控宿主对PSMs防御机制的适应能力。本研究结果揭示了肠道微生物组在植物-昆虫互作中赋予宿主适应PSMs能力的重要作用。