Microbial control over host diet selection

Abstract

Diet selection is a fundamental aspect of animal behavior with numerous ecological and evolutionary implications. While the underlying mechanisms are complex, the availability of essential dietary nutrients can strongly influence diet selection behavior. The gut microbiome has been shown to metabolize many of these same nutrients, leading to the untested hypothesis that intestinal microbiota may influence diet selection. Here we show that germ-free mice colonized by gut microbiota from three rodent species with distinct foraging strategies differentially selected diets that varied in macronutrient composition. Specifically, we found that herbivore-conventionalized mice voluntarily selected a higher protein:carbohydrate ratio diet, while omnivore- and carnivore-conventionalized mice selected a lower P:C ratio diet. In support of the long-standing hypothesis that tryptophan - the essential amino acid precursor of serotonin - serves as a peripheral signal regulating diet selection, bacterial genes involved in tryptophan metabolism and plasma tryptophan availability prior to the selection trial were significantly correlated with subsequent voluntary carbohydrate intake. Finally, herbivore-conventionalized mice exhibited larger intestinal compartments associated with microbial fermentation, broadly reflecting the intestinal morphology of their donor species. Together, these results demonstrate that gut microbiome can influence host diet selection behavior, perhaps by mediating the availability of essential amino acids, thereby revealing a novel mechanism by which the gut microbiota can influence host foraging behavior. SIGNIFICANCEThe behavior of diet choice or diet selection can have wide-reaching implications, scaling from individual animals to ecological and evolutionary processes. Previous work in this area has largely ignored the potential for intestinal microbiota to modulate these signals. This notion has been highly speculated for years but has not yet been explicitly tested. Here we show that germ-free mice colonized by differential microbiomes (from wild rodents with varying natural feeding strategies) exhibited significant differences in their voluntary dietary selection. Specifically, differences in voluntary carbohydrate selection were associated with plasma amino acid levels and bacterial genes involved in the metabolism of tryptophan. Together, these results demonstrate a role for the microbiome in host nutritional physiology and behavior.