Commensal bacteria and essential amino acids control food choice behavior and reproduction

Choosing the right nutrients to consume is essential to health and wellbeing across species. However, the factors that influence these decisions are poorly understood. This is particularly true for dietary proteins, which are important determinants of lifespan and reproduction. We show that in Drosophila melanogaster, essential amino acids (eAAs) and the concerted action of the commensal bacteria Acetobacter pomorum and Lactobacilli are critical modulators of food choice. Using a chemically defined diet, we show that the absence of any single eAA from the diet is sufficient to elicit specific appetites for amino acid (AA)-rich food. Furthermore, commensal bacteria buffer the animal from the lack of dietary eAAs: both increased yeast appetite and decreased reproduction induced by eAA deprivation are rescued by the presence of commensals. Surprisingly, these effects do not seem to be due to changes in AA titers, suggesting that gut bacteria act through a different mechanism to change behavior and reproduction. Thus, eAAs and commensal bacteria are potent modulators of feeding decisions and reproductive output. This demonstrates how the interaction of specific nutrients with the microbiome can shape behavioral decisions and life history traits.

Author summary What animals, including humans, choose to eat has a tremendous impact on health and wellbeing. Though intake of dietary proteins and amino acids is essential for animals, excessive consumption of these nutrients is known to have detrimental effects. Many animals, therefore, execute precise control over the intake of these key nutrients. However, the factors controlling protein appetite are poorly understood. Here, we show that in the vinegar fly Drosophila melanogaster, essential amino acids and gut bacteria are key modulators of protein appetite. Lack of any one essential amino acid from the diet produces a strong and specific appetite for proteinaceous or amino acid–rich food. However, flies with an appropriate microbiome do not develop this protein appetite. Specifically, two gut bacteria species, Acetobacter pomorum and Lactobacilli, work together to suppress protein appetite. Furthermore, we show that flies lacking dietary essential amino acids have reduced reproductive output, an effect which is also rescued by gut bacteria. Finally, based on metabolite measurements, we propose that the influence of bacteria on host physiology and behavior is not mediated by changing amino acid levels. Our study demonstrates how the interaction of specific nutrients with the microbiome can shape behavior and animal fitness and suggests that they do so through a novel mechanism.