The mammalian gut microbiome plays an important role in host nutrient and xenobiotic metabolism. In herbivorous rodents, gut microbial communities facilitate the intake of diets that contain plant secondary compounds. It is unknown whether the microbiome of omnivorous rodents participates in degradation of toxins ingested with an insect-based diet. Black-eared mice (Peromyscus melanotis) are an interesting system to advance our understanding of microbial mechanisms of detoxification, because they seasonally feed on monarch butterflies (Danaus plexippus) despite the monarch’s high toxicity. During early development, monarch butterflies sequester toxic cardenolides, which are potent secondary metabolites that inhibit the animal enzyme sodium-potassium ATPase, affecting the cardiovascular system of vertebrates. Our aim was to explore the relationship between cardenolide intake and the microbiome of wild mice. We asked Does the microbial community of black-eared mice change with intake of toxic monarch butterflies? We conducted fieldwork in monarchs’ overwintering sites in Michoacán, Mexico. We live-trapped and collected fecal samples from black-eared mice during two seasons, with and without monarchs. We conducted feeding trials consisting of feeding black-eared mice exclusively with monarchs over 48h. Changes in fecal microbial communities were determined through 16S rRNA gene sequencing.
Results/Conclusions
Insect DNA metabarcoding confirmed that wild black-eared mice were feeding on monarch butterflies in Mexican overwintering sites. We also confirmed, through chromatography analysis, that the body of these migratory monarch butterflies still contained high cardenolide levels. We found that during the monarch season, black-eared mice showed higher gut bacterial diversity (Kruskal-Wallis H= 10.7, p= 0.001) compared to the no-monarch season. Microbial structure also exhibited significant seasonal shifts from the no-monarch season to the season when monarchs were present (PERMANOVA pseudo-F1,32= 2.6, p= 0.001). Microbes belonging to Ruminococcaceae and Lachnospiraceae were enriched during the monarch season. In feeding trials, mice also experienced shifts in their microbial communities. After feeding exclusively on monarch butterflies, mice showed an enrichment in microbes belonging to Lactobacillus, Lachnospiraceae, Enterobacteriaceae, and Muribaculaceae. We found that the intake of chemically defended monarch butterflies restructured the gut microbiome of black-eared mice. In the future, we plan to use metagenomic techniques to probe the function of the microbiome with respect to degradation of cardenolides.