How gut microbiome interactions affect nutritional traits of Drosophila melanogaster

Most research on the impact of the gut microbiome on animal nutrition is designed to identify the effects of single microbial taxa and single metabolites of microbial origin, without considering the potentially complex network of interactions among co-occurring microorganisms. Here, we investigate how different microbial associations and their fermentation products affect host nutrition, using Drosophila melanogaster colonized with three gut microorganisms (the bacteria Acetobacter fabarum and Lactobacillus brevis and the yeast Hanseniaspora uvarum) in all seven possible combinations. Some microbial effects on host traits could be attributed to single taxa (e.g. yeast-mediated reduction of insect development time), while other effects were sex-specific and driven by among-microbe interactions (e.g. male lipid content determined by interactions between the yeast and both bacteria). Parallel analysis of nutritional indices of microbe-free flies administered different microbial fermentation products (acetic acid, acetoin, ethanol and lactic acid) revealed a single consistent effect: that the lipid content of both male and female flies is reduced by acetic acid. This effect was recapitulated in male flies colonized with both yeast and Acetobacter, but not for any microbial treatment in females nor in males with other microbial complements. These data suggest that the effect of microbial fermentation products on host nutritional status is strongly context-dependent, with respect to both the combination of associated microorganisms and host sex. Taken together, our findings demonstrate that among-microbe interactions can play a critically important role in determining the physiological outcome of host-microbiome interactions in Drosophila and, likely, in other animal hosts.