Core bacterial and host fruit-specific yeast microbiota in a polyphagous fly pest

Holometabolous polyphagous insects undergo metamorphosis and exploit multiple host plants, exposing them to highly variable ecological conditions across both life stages and host plants. Whether these insects harbor a stable core microbiota, a life stage- or a host plant-specific microbiota remains open questions. Here, we characterized fungal and bacterial communities associated with Drosophila suzukii across life stages (larvae, pupae, and emerging flies) and host fruits (cherry, blackberry, and strawberry) 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. First, we identified that yeasts, but not bacteria, were strongly structured among host fruits. Bacteria and filamentous fungi were shared across fruits, constituting a fruit core microbiota dominated by Gluconobacter cerinus, Tatumella sp., and Cladosporium spp. In contrast, yeast were rather fruit-specific: the genera Hanseniaspora and Pichia were mostly associated with cherries and strawberries, contrary to Metschnikowia with blackberries. Second, we found that fungal, but not bacterial, communities of D. suzukii were structured among host fruits. D. suzukii harbored a core bacterial microbiota composed of G. cerinus and a niche-specific (host plant-specific) microbiota composed of yeasts: Hanseniaspora was typical in individuals related to cherry and strawberry, whereas Metschnikowia to blackberry. We also verified that individuals from artificial laboratory infestations and natural field infestations harbored similar microbial communities when they developed under the same laboratory conditions. 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 metacommunity approaches to investigate tripartite interactions among insects, host plants, and microbiota.IMPORTANCEThe role of 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 in holometabolous species that experience 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, D. suzukii harbors 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 insect-microbe interactions.