Core Bacterial and Host Fruit-Specific Yeast Microbiota in a Polyphagous Fly Pest

Holometabolous polyphagous insects undergo complete metamorphosis and exploit multiple host plants, exposing them to highly variable ecological conditions across both life stages and host plants. Whether these species, like specialist ones, harbour a stable core microbiota, or whether life stages or host plants act as the primary drivers of microbiota assembly remain open questions. Here, we characterized the fungal and bacterial communities associated with Drosophila suzukii across life stages and host fruits using 16S and ITS metabarcoding. We tested the relative influence of life stage and host fruit on microbiota composition, using community and network-based analyses. We first identified that host fruit significantly structured fungal communities, but not bacterial ones. Yeast communities were rather fruit-specific: Hanseniaspora and Pichia mostly associated with cherries and strawberries, contrary to Metschnikowia with blackberries. In contrast, bacteria and filamentous fungi were shared across fruits, constituting for fruits a core microbiota dominated by Gluconobacter cerinus, Tatumella and Cladosporium. Second, we found that both bacterial and fungal D. suzukii communities were structured by life stage, and that fungal, but not bacterial communities, were also structured by host fruits. D. suzukii individuals harboured a core bacteria composed of G. cerinus and a niche-specific microbiota composed of yeasts: Hanseniaspora typical in individuals related to cherry and strawberry, and Metschnikowia to blackberry. Components of both core and niche-specific microbiota were most likely horizontally acquired by D. suzukii from host fruits. Taken together our results underline the importance of meta-community approaches to investigate tripartite interactions among insects, host plants and microbiota. IMPORTANCEThe role of gut microbiota in mediating interactions between phytophagous insects and their host plants has been well illustrated in specialist species. However, it has been less comprehensively studied in polyphagous species, which infest multiple host plants, and across life stages for holometabolous species experiencing separate ecological niches through development. We tested the existence of a core, a niche-specific and a stage-specific microbiota in a polyphagous holometabolous species, D. suzukii. We examined both fungal and bacterial communities in larvae, pupae and emerging flies infesting three host fruits. Our results showed first that the assembly of bacteria, filamentous fungi and yeasts on fruits is driven by different ecological processes. Second, that D. suzukii harbours a core bacterial microbiota, a niche-specific microbiota constituted by yeasts and no stage-specific microbiota. Our study emphasizes the importance of considering jointly the assembly of host plant and polyphagous insect microbial communities to better understand the ecology and evolution of insect-microbe interactions.