Ana Grande Mateu, Courtney A. Hofman, Katerina Harvati, Louise T. Humphrey, Mario Menéndez, Richard W. Wrangham, Dušan Mihailović, Kathryn Weedman Arthur, Cody Parker, Barbara Teßmann, Jay T. Stock, Isabelle Crevecoeur, Michael J. Walker, Catherine C. Bauer, Christina Warinner, Cosimo Posth, Mirjana Roksandic, Victoria E. Gibbon, Love Dalén, Dorothée G. Drucker, Amanda G. Henry, Manuel R. González Morales, Floyd E. Dewhirst, Kathrin Nägele, Christophe Cupillard, Michael Francken, Irina M. Velsko, Johannes Krause, Sofía Rodríguez Moroder, Sandra Sázelová, Katerina Guschanski, Rita M. Austin, James A. Fellows Yates, J. Carlos Díez Fernández-Lomana, Marta Díaz-Zorita Bonilla, Hélène Rougier, Cecil M. Lewis, Marco Peresani, Robert C. Power, Krithivasan Sankaranarayanan, Domingo C. Salazar-García, Lawrence Guy Straus, Alexander Herbig, Jiří Svoboda, John W. Arthur, Elena Escribano Escrivá, Matthew C. Curtis, Franziska Aron, Allison E. Mann, Lab Chronoenvironm, Partenaires INRAE, European Commission, De la Préhistoire à l'Actuel : Culture, Environnement et Anthropologie (PACEA), Université de Bordeaux (UB)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Chrono-environnement - CNRS - UBFC (UMR 6249) (LCE), Centre National de la Recherche Scientifique (CNRS)-Université de Franche-Comté (UFC), Université Bourgogne Franche-Comté [COMUE] (UBFC)-Université Bourgogne Franche-Comté [COMUE] (UBFC), Fellows Yates, James A [0000-0001-5585-6277], Velsko, Irina M [0000-0001-9810-9917], Hofman, Courtney A [0000-0002-6808-3370], Parker, Cody E [0000-0001-5528-4299], Mann, Allison E [0000-0001-7170-6017], Arthur, Kathryn Weedman [0000-0003-2955-6080], Arthur, John W [0000-0002-4968-5843], Bauer, Catherine C [0000-0002-2281-0501], Crevecoeur, Isabelle [0000-0002-1781-3206], Cupillard, Christophe [0000-0002-8567-3540], Curtis, Matthew C [0000-0003-4692-3241], Dalén, Love [0000-0001-8270-7613], Díaz-Zorita Bonilla, Marta [0000-0002-1697-0111], Díez Fernández-Lomana, J Carlos [0000-0002-3856-1837], Francken, Michael [0000-0001-6336-2111], Gibbon, Victoria E [0000-0001-7875-3297], González Morales, Manuel R [0000-0001-7277-7837], Henry, Amanda G [0000-0002-2923-4199], Humphrey, Louise [0000-0003-3595-0543], Menéndez, Mario [0000-0002-2421-480X], Mihailović, Dušan [0000-0002-8607-8196], Peresani, Marco [0000-0001-6562-6336], Roksandic, Mirjana [0000-0003-0291-6357], Rougier, Hélène [0000-0003-0358-0285], Sázelová, Sandra [0000-0002-7326-8134], Straus, Lawrence Guy [0000-0003-0348-3338], Svoboda, Jiří [0000-0003-4256-9708], Teßmann, Barbara [0000-0002-3122-4707], Walker, Michael J [0000-0003-4359-7436], Power, Robert C [0000-0001-7425-5709], Lewis, Cecil M [0000-0002-2198-3427], Guschanski, Katerina [0000-0002-8493-5457], Wrangham, Richard W [0000-0003-0435-2209], Dewhirst, Floyd E [0000-0003-4427-7928], Krause, Johannes [0000-0001-9144-3920], Herbig, Alexander [0000-0003-1176-1166], Warinner, Christina [0000-0002-4528-5877], and Apollo - University of Cambridge Repository
Significance The microbiome plays key roles in human health, but little is known about its evolution. We investigate the evolutionary history of the African hominid oral microbiome by analyzing dental biofilms of humans and Neanderthals spanning the past 100,000 years and comparing them with those of chimpanzees, gorillas, and howler monkeys. We identify 10 core bacterial genera that have been maintained within the human lineage and play key biofilm structural roles. However, many remain understudied and unnamed. We find major taxonomic and functional differences between the oral microbiomes of Homo and chimpanzees but a high degree of similarity between Neanderthals and modern humans, including an apparent Homo-specific acquisition of starch digestion capability in oral streptococci, suggesting microbial coadaptation with host diet., The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine–platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.