Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System

Abstract

Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab.

Author Summary

All animals are associated with large consortia of non-pathogenic microbes. Most of these “microbiomes” are not well characterized despite their importance for many aspects of host biology including human and animal health and the agricultural impact of pest species. The fruit fly Drosophila melanogaster provides a powerful experimental model for investigating the dynamics and consequences of animal–microbial interactions. However, it is not clear whether the model bacteria studied in the lab are representative of natural microbial consortia. To establish an ecological and comparative background for experimental studies, we have conducted a global survey of bacterial communities associated with natural populations of 14 species of Drosophila and related genera. Despite the taxonomic and ecological diversity of these species, we find that they are associated with the same dominant bacterial groups. Based on our results, we propose a model of microbiome assembly where its composition is circumscribed by host diet and physiology but, within those limits, is highly dependent on chance environmental encounters. Consistent with this model, the microbiomes of wild flies differ significantly from those of laboratory strains, suggesting that experimental studies should be extended to include the bacteria that are most prevalent in natural communities.