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.

Integrating nutrition and immunology: A new frontier

“…(Chandler et al, 2011) assessed the importance of host diet and host species in shaping microbiome composition in flies. They showed that whereas taxonomically-and geographically-distant fly populations, collected from various food sources, have very different microbiome compositions, when maintained on the same type of food they developed similar microbiomes.…”

The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis

“…Nevertheless, the gut microbiota does not simply reflect the microorganisms in the food, but can be dominated by bacteria that are taxonomically distinct from bacteria in other environments (Ley et al, 2008b;Tamames et al, 2010;Chandler et al, 2011). The distinctiveness of the gut microbiota can be attributed to the ecological conditions in the gut, including regions with extreme pH or redox potential, biologically active compounds (for example, digestive enzymes, immune effectors) and disturbance (for example, bulk flow of food, production of mucus or other extracellular secretions, epithelial cell turnover) (Karasov and Douglas, 2013).…”

“…The gut microbiota in these insects has been reported to include Proteobacteria (especially Acetobacteraceae and Enterobacteriaceae) and Firmicutes of the order Lactobacillales (notably Lactobacillus and Enterococcus species). Despite regional variation in conditions (pH, redox potential and so on) in the gut (Shanbhag and Tripathi, 2009), bacteria occur in the crop, midgut and hindgut, with densities up to 10 6 cells per fly (Corby-Harris et al, 2007;Cox and Gilmore, 2007;Ren et al, 2007;Roh et al, 2008;Sharon et al, 2010;Chandler et al, 2011;Storelli et al, 2011;Wong et al, 2011). Elimination of the gut bacteria can result in delayed larval development, altered lifespan and changes in nutrient allocation attributable to disruption in insect insulin signaling (Brummel et al, 2004;Shin et al, 2011;Storelli et al, 2011;Ridley et al, 2012).…”

Kin recognition in Drosophila: the importance of ecology and gut microbiota

“…In Drosophila sp., gut bacteria communities vary widely according to ecology, however, similarities may exist between individuals/species feeding on the same food source (Chandler et al, 2011). In Drosophila melanogaster, slight changes in the composition of cuticular hydrocarbons significantly alter mating success (Scott et al, 2011).…”