Interspecies Interactions Determine the Impact of the Gut Microbiota on Nutrient Allocation in Drosophila melanogaster

Abstract

ABSTRACTThe animal gut is perpetually exposed to microorganisms, and this microbiota affects development, nutrient allocation, and immune homeostasis. A major challenge is to understand the contribution of individual microbial species and interactions among species in shaping these microbe-dependent traits. Using theDrosophila melanogastergut microbiota, we tested whether microbe-dependent performance and nutritional traits ofDrosophilaare functionally modular, i.e., whether the impact of each microbial taxon on host traits is independent of the presence of other microbial taxa. Gnotobiotic flies were constructed with one or a set of five of theAcetobacterandLactobacillusspecies which dominate the gut microbiota of conventional flies (Drosophilawith untreated microbiota). Axenic (microbiota-free) flies exhibited prolonged development time and elevated glucose and triglyceride contents. The low glucose content of conventional flies was recapitulated in gnotobioticDrosophilaflies colonized with any of the 5 bacterial taxa tested. In contrast, the development rates and triglyceride levels in monocolonized flies varied depending on the taxon present:Acetobacterspecies supported the largest reductions, while mostLactobacillusspecies had no effect. Only flies with bothAcetobacterandLactobacillushad triglyceride contents restored to the level in conventional flies. This could be attributed to two processes:Lactobacillus-mediated promotion ofAcetobacterabundance in the fly and a significant negative correlation between fly triglyceride content andAcetobacterabundance. We conclude that the microbial basis of host traits varies in both specificity and modularity; microbe-mediated reduction in glucose is relatively nonspecific and modular, while triglyceride content is influenced by interactions among microbes.