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

Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals Sophie Teulleta,#, Marie-Ka Tilaka, Amandine Magdeleinea, Roxane Schaubb,c, Nora M. Weyerd, Wendy Panainod,e, Andrea Fullerd, William. J. Loughryf, Nico L. Avenantg, Benoit de Thoisyh,i, Guillaume Borrelj and Frédéric Delsuca,# aInstitut des Sciences de l’Evolution de Montpellier (ISEM), Univ Montpellier, CNRS, IRD, Montpellier, France bCIC AG/Inserm 1424, Centre Hospitalier de Cayenne Andrée Rosemon, Cayenne, French Guiana cTropical Biome and immunopathology, Université de Guyane, Labex CEBA, DFR Santé, Cayenne, French Guiana dBrain Function Research Group, School of Physiology, University of the Witwatersrand, Johannesburg, South Africa eCentre for African Ecology, School of Animals, Plant, and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa fDepartment of Biology, Valdosta State University, Valdosta, GA, USA gNational Museum and Centre for Environmental Management, University of the Free State, Bloemfontein, South Africa hInstitut Pasteur de la Guyane, Cayenne, French Guiana, France iKwata NGO, Cayenne, French Guiana, France jInstitut Pasteur, Université Paris Cité, UMR CNRS 6047, Evolutionary Biology of the Microbial Cell, Paris, France #Corresponding authors: sophie.teullet@umontpellier.fr; frederic.delsuc@umontpellier.fr 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 USA. 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 t