Widespread extinctions of co-diversified primate gut bacterial symbionts from humans

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  • Jon G. Sanders
    Cornell University
  • Daniel D. Sprockett
    Cornell University
  • Yingying Li
    University of Pennsylvania
  • Deus Mjungu
    Gombe Stream Research Center
  • Elizabeth V. Lonsdorf
    Emory University
  • Jean-Bosco N. Ndjango
    University of Kisangani
  • Alexander V. Georgiev
  • John A. Hart
    Lukuru Wildlife Research Foundation, Kinshasa
  • Crickette M. Sanz
    Washington University, St Louis
  • David B. Morgan
    Lincoln Park Zoo, Chicago
  • Martine Peeters
    Université de Montpellier
  • Beatrice H. Hahn
    University of Pennsylvania
  • Andrew H. Moeller
    Cornell University
Humans and other primates harbour complex gut bacterial communities that influence health and disease, but the evolutionary histories of these symbioses remain unclear. This is partly due to limited information about the microbiota of ancestral primates. Here, using phylogenetic analyses of metagenome-assembled genomes (MAGs), we show that hundreds of gut bacterial clades diversified in parallel (that is, co-diversified) with primate species over millions of years, but that humans have experienced widespread losses of these ancestral symbionts. Analyses of 9,460 human and non-human primate MAGs, including newly generated MAGs from chimpanzees and bonobos, revealed significant co-diversification within ten gut bacterial phyla, including Firmicutes, Actinobacteriota and Bacteroidota. Strikingly, ~44% of the co-diversifying clades detected in African apes were absent from available metagenomic data from humans and ~54% were absent from industrialized human populations. In contrast, only ~3% of non-co-diversifying clades detected in African apes were absent from humans. Co-diversifying clades present in both humans and chimpanzees displayed consistent genomic signatures of natural selection between the two host species but differed in functional content from co-diversifying clades lost from humans, consistent with selection against certain functions. This study discovers host-species-specific bacterial symbionts that predate hominid diversification, many of which have undergone accelerated extinctions from human populations.
Original languageEnglish
Pages (from-to)1039-1050
Number of pages12
JournalNature Microbiology
Issue number6
Early online date11 May 2023
Publication statusPublished - Jun 2023

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