Functional host-specific adaptation of the intestinal microbiome in hominids

M. C. Rühlemann (), C. Bang, J. F. Gogarten, B. M. Hermes, M. Groussin, S. Waschina, M. Poyet, M. Ulrich, C. Akoua-Koffi, T. Deschner, J. J. Muyembe-Tamfum, M. M. Robbins, M. Surbeck, R. M. Wittig, K. Zuberbühler, J. F. Baines, F. H. Leendertz and A. Franke ()
Additional contact information
M. C. Rühlemann: Kiel University
C. Bang: Kiel University
J. F. Gogarten: University of Greifswald
B. M. Hermes: Max Planck Institute for Evolutionary Biology
M. Groussin: Kiel University
S. Waschina: Kiel University
M. Poyet: Kiel University
M. Ulrich: Helmholtz-Centre for Infection Research (HZI)
C. Akoua-Koffi: Alassane Ouattara University / University Teaching Hospital of Bouaké
T. Deschner: University of Osnabrück
J. J. Muyembe-Tamfum: National Laboratory of Public Health
M. M. Robbins: Max Planck Institute for Evolutionary Anthropology
M. Surbeck: Harvard University
R. M. Wittig: Institute of Cognitive Sciences, CNRS UMR5229 University Lyon 1
K. Zuberbühler: University of Neuchatel
J. F. Baines: Max Planck Institute for Evolutionary Biology
F. H. Leendertz: Helmholtz-Centre for Infection Research (HZI)
A. Franke: Kiel University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Fine-scale knowledge of the changes in composition and function of the human gut microbiome compared that of our closest relatives is critical for understanding the evolutionary processes underlying its developmental trajectory. To infer taxonomic and functional changes in the gut microbiome across hominids at different timescales, we perform high-resolution metagenomic-based analyzes of the fecal microbiome from over two hundred samples including diverse human populations, as well as wild-living chimpanzees, bonobos, and gorillas. We find human-associated taxa depleted within non-human apes and patterns of host-specific gut microbiota, suggesting the widespread acquisition of novel microbial clades along the evolutionary divergence of hosts. In contrast, we reveal multiple lines of evidence for a pervasive loss of diversity in human populations in correlation with a high Human Development Index, including evolutionarily conserved clades. Similarly, patterns of co-phylogeny between microbes and hosts are found to be disrupted in humans. Together with identifying individual microbial taxa and functional adaptations that correlate to host phylogeny, these findings offer insights into specific candidates playing a role in the diverging trajectories of the gut microbiome of hominids. We find that repeated horizontal gene transfer and gene loss, as well as the adaptation to transient microaerobic conditions appear to have played a role in the evolution of the human gut microbiome.

Date: 2024
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DOI: 10.1038/s41467-023-44636-7

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