High-tannin food enhances spatial memory and scatter-hoarding via the microbiota-gut-brain axis of rodents

The mutually beneficial coevolutionary relationships between rodents and plant seeds have been a hot topic of research in plant-animal relationships. Seed tannins are important secondary metabolites of plants that regulate food-hoarding behavior of rodents; however, the underlying molecular mechanisms are not yet clear. In this study, we investigate whether and how seed tannins improve spatial memory and regulate the hoarding behavior of Tamias sibiricus by altering their gut microbiota. We show that acorn tannins not only improve spatial memory but enhance scatter-hoarding of T. sibiricus. Changes in the composition and function of the gut microbiota in response to tannins from acorns are closely related to these improvement and enhancement. Metabonomic analyses evidence the role of gut isovaleric acid andisobutyric acid as well as serum L-tryptophan in mediating spatial memory of T. sibiricus via the gut microbiota. The hippocampus proteome provides further evidence for the microbiota-gut-brain axis in regulating spatial memory and scatter-hoarding of animals. Our study is likely the first to report that plant secondary metabolites improve hippocampal function and spatial memory, and ultimately modulate food-hoarding behavior via the microbiota-gut-brain axis. Our study provides a new direction for the study of the mutualistic interaction between plant secondary metabolites and food-hoarding rodents.