Functional host-specific adaptation of the intestinal microbiome in hominids
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 microbiom...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-44636-7 |
| _version_ | 1827388321910751232 |
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| author | 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 A. Franke |
| author_facet | 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 A. Franke |
| author_sort | M. C. Rühlemann |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-08T16:16:11Z |
| format | Article |
| id | doaj.art-42b4e16b34fc42da97642083ef5f5f9c |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T16:16:11Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-42b4e16b34fc42da97642083ef5f5f9c2024-01-07T12:33:12ZengNature PortfolioNature Communications2041-17232024-01-0115111710.1038/s41467-023-44636-7Functional host-specific adaptation of the intestinal microbiome in hominidsM. C. Rühlemann0C. Bang1J. F. Gogarten2B. M. Hermes3M. Groussin4S. Waschina5M. Poyet6M. Ulrich7C. Akoua-Koffi8T. Deschner9J. J. Muyembe-Tamfum10M. M. Robbins11M. Surbeck12R. M. Wittig13K. Zuberbühler14J. F. Baines15F. H. Leendertz16A. Franke17Institute of Clinical Molecular Biology, Kiel UniversityInstitute of Clinical Molecular Biology, Kiel UniversityApplied Zoology and Nature Conservation, University of GreifswaldEvolutionary Genomics, Max Planck Institute for Evolutionary BiologyInstitute of Clinical Molecular Biology, Kiel UniversityNutriinformatics Research Group, Institute for Human Nutrition and Food Science, Kiel UniversityInstitute of Experimental Medicine, Kiel UniversityHelmholtz Institute for One Health, Helmholtz-Centre for Infection Research (HZI)Training and Research Unit for in Medical Sciences, Alassane Ouattara University / University Teaching Hospital of BouakéComparative BioCognition, Institute of Cognitive Science, University of OsnabrückNational Institute for Biomedical Research, National Laboratory of Public HealthDepartment of Primate Behavior and Evolution, Max Planck Institute for Evolutionary AnthropologyDepartment of Human Evolutionary Biology, Harvard UniversityInstitute of Cognitive Sciences, CNRS UMR5229 University Lyon 1Institute of Biology, University of NeuchatelEvolutionary Genomics, Max Planck Institute for Evolutionary BiologyHelmholtz Institute for One Health, Helmholtz-Centre for Infection Research (HZI)Institute of Clinical Molecular Biology, Kiel UniversityAbstract 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.https://doi.org/10.1038/s41467-023-44636-7 |
| spellingShingle | 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 A. Franke Functional host-specific adaptation of the intestinal microbiome in hominids Nature Communications |
| title | Functional host-specific adaptation of the intestinal microbiome in hominids |
| title_full | Functional host-specific adaptation of the intestinal microbiome in hominids |
| title_fullStr | Functional host-specific adaptation of the intestinal microbiome in hominids |
| title_full_unstemmed | Functional host-specific adaptation of the intestinal microbiome in hominids |
| title_short | Functional host-specific adaptation of the intestinal microbiome in hominids |
| title_sort | functional host specific adaptation of the intestinal microbiome in hominids |
| url | https://doi.org/10.1038/s41467-023-44636-7 |
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