Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals

Abstract

ABSTRACT In mammals, myrmecophagy (ant and termite consumption) represents a striking example of dietary convergence. This trait evolved independently at least five times in placentals with myrmecophagous species comprising aardvarks, anteaters, some armadillos, pangolins, and aardwolves. The gut microbiome plays an important role in dietary adaptation, and previous analyses of 16S rRNA metabarcoding data have revealed convergence in the composition of the gut microbiota among some myrmecophagous species. However, the functions performed by these gut bacterial symbionts and their potential role in the digestion of prey chitinous exoskeletons remain open questions. Using long- and short-read sequencing of fecal samples, we generated 29 gut metagenomes from nine myrmecophagous and closely related insectivorous species sampled in French Guiana, South Africa, and the United States. From these, we reconstructed 314 high-quality bacterial genome bins of which 132 carried chitinase genes, highlighting their potential role in insect prey digestion. These chitinolytic bacteria belonged mainly to the family Lachnospiraceae, and some were likely convergently recruited in the different myrmecophagous species as they were detected in several host orders (i.e., Enterococcus faecalis , Blautia sp.), suggesting that they could be directly involved in the adaptation to myrmecophagy. Others were found to be more host-specific, possibly reflecting phylogenetic constraints and environmental influences. Overall, our results highlight the potential role of the gut microbiome in chitin digestion in myrmecophagous mammals and provide the basis for future comparative studies performed at the mammalian scale to further unravel the mechanisms underlying the convergent adaptation to myrmecophagy. Importance Myrmecophagous mammals are specialized in the consumption of ants and/or termites. They do not share a direct common ancestor and evolved convergently in five distinct placental orders raising questions about the underlying adaptive mechanisms involved and the relative contribution of natural selection and phylogenetic constraints. Understanding how these species digest their prey can help answer these questions. More specifically, the role of their gut microbial symbionts in the digestion of the insect chitinous exoskeleton has not been investigated in all myrmecophagous orders. We generated 29 new gut metagenomes from nine myrmecophagous species to reconstruct more than 300 bacterial genomes in which we identified chitin-degrading enzymes. Studying the distribution of these chitinolytic bacteria among hosts revealed both shared and specific bacteria between ant-eating species. Overall, our results highlight the potential role of gut symbionts in the convergent dietary adaptation of myrmecophagous mammals and the evolutionary mechanisms shaping their gut microbiota.