Bacterial transmission within social groups shapes the underexplored gut microbiome in the lemur Indri indri

Abstract

The Indri indri is a critically endangered lemur species that has not successfully been maintained or bred under human care. Investigating this lemur's virtually unexplored gut microbiome will deepen our understanding of the species' health determinants and inform conservation efforts. Through metagenomic assembly and integration into an updated reference database, we found the I. indri fecal microbiome remains largely uncultivated (cultivated species representing <0.1% relative abundance) and is largely specific to this primate species. After reconstructing 342 metagenome-assembled genomes encompassing 48 candidate species from a total of 22 samples (18 of which newly sequenced), we substantially improved microbiome mappability to 85% on average and found evidence for a proportionally large core microbiome. Social group membership emerged as the main determinant of both their taxonomic and functional gut microbiome composition. Using strain-level profiling, we detected extensive microbiome transmission within social groups, suggesting physical interaction is key in promoting microbiome acquisition. Strain sharing rates were highest between mothers and their offspring. Intergroup strain sharing was minimal and inversely correlated with geographical distance, aligning with the rare intergroup interactions and stable territory occupancy coupled with ongoing habitat fragmentation. No evidence of microbiome acquisition through geophagy was detected. These findings underscore the profound influence of social structure on microbiome transmission and composition in I. indri, and highlight the importance of considering social dynamics into research and conservation strategies.

This work was supported by the European Research Council (ERC-CoG microTOUCH-101045015) to NS, Knowledge Generation Project (PID2022-139328OA-I00) from the Spanish Ministry of Science and Innovation to MV-C, Beatriz Galindo Junior fellowship (BG22/00172) from the Spanish Ministry of Universities to MV-C, La Caixa Junior Leader fellowship from La Caixa Foundation (ID 100010434, code LCF/BQ/PI24/12040001) to MV-C.