Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals
\n\nSophie 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,#
\n\naInstitut des Sciences de l’Evolution de Montpellier (ISEM), Univ Montpellier, CNRS, IRD, Montpellier, France
\n\nbCIC AG/Inserm 1424, Centre Hospitalier de Cayenne Andrée Rosemon, Cayenne, French Guiana
\n\ncTropical Biome and immunopathology, Université de Guyane, Labex CEBA, DFR Santé, Cayenne, French Guiana
\n\ndBrain Function Research Group, School of Physiology, University of the Witwatersrand, Johannesburg, South Africa
\n\neCentre for African Ecology, School of Animals, Plant, and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa
\n\nfDepartment of Biology, Valdosta State University, Valdosta, GA, USA
\n\ngNational Museum and Centre for Environmental Management, University of the Free State, Bloemfontein, South Africa
\n\nhInstitut Pasteur de la Guyane, Cayenne, French Guiana, France
\n\niKwata NGO, Cayenne, French Guiana, France
\n\njInstitut Pasteur, Université Paris Cité, UMR CNRS 6047, Evolutionary Biology of the Microbial Cell, Paris, France
\n\n#Corresponding authors: sophie.teullet@umontpellier.fr; frederic.delsuc@umontpellier.fr
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Abstract
\n\nIn 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 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.
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Main figures and corresponding datasets
\n\nFigure_1_dataset.zip contains:
\n\nFigure_2_dataset.zip contains:
\n\nFigure_3_dataset.zip contains:
\n\nFigure_4_dataset.zip contains:
\n\nTable_1_sample_infos.xls: Detailed sample information for the 33 fecal samples collected. N.B.: Diet was determined based on field observations (i.e., dissections) and the literature.
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Supplementary results
\n\nSupplementary_results_Teullet_etal_2023.zip includes a comparison of genome statistics of the selected bins reconstructed from the long-read vs the short-read datasets, a phylogeny of the set of selected bins before dereplication (n = 407) and a comparison of the distribution of shared and specific genome bins carrying GH18 among host orders.
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Supplementary material
\n\nSupplementary_material_Teullet_etal_2023.zip contains
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Assemblies
\n\nLong-read_metagenomic_assemblies_polished.zip contains the 31 long-read metagenomes assembled with metaFlye strain v2.9 and polished with short reads using Pilon v1.4, which were used for binning.
\n\nLong-read_metagenomic_assemblies_not_polished.zip contains the 33 long-read metagenomes assembled with metaFlye strain v2.9 before polishing.
\n\nShort-read_metagenomic_assemblies.zip contains the 31 short-read metagenomes assembled with metaSPAdes and MEGAHIT.
\n\nN.B:
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Binning: genome bins and dereplication results
\n\nHigh-quality_selected_bins_dereplicated.zip contains the 314 high quality selected bins (>90% completion, <5% redundancy) reconstructed from long- and short-read metagenomes with metaBAT2 and dereplicated with dRep at 98% ANI.
\n\nmetaBAT2_short-read_assemblies_bins.zip contains all bins reconstructed from the short-read assemblies with metaBAT2 (i.e., output of metaBAT2).
\n\nmetaBAT2_long-read_assemblies_bins.zip contains all bins reconstructed from the long-read polished assemblies with metaBAT2 (i.e., output of metaBAT2).
\n\nOutput_dRep_98ANI_407_bins_long-short-reads.zip contains the output of the dereplication analysis done on the set of 407 high-quality selected genome bins reconstructed from long- (n = 201) and short-read (n = 206; labeled "spad") metagenomes. It was performed with dRep using default parameters. After this step, the final dataset included 314 high-quality non-redundant genome bins. This folder includes:
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