The evolution and changing ecology of the African hominid oral microbiome
View ORCID ProfileJames A. Fellows Yates, View ORCID ProfileIrina M. Velsko, Franziska Aron, Cosimo Posth, View ORCID ProfileCourtney A. Hofman, Rita M. Austin, View ORCID ProfileCody E. Parker, View ORCID ProfileAllison E. Mann, Kathrin Nägele, View ORCID ProfileKathryn Weedman Arthur, View ORCID ProfileJohn W. Arthur, View ORCID ProfileCatherine C. Bauer, View ORCID ProfileIsabelle Crevecoeur, View ORCID ProfileChristophe Cupillard, View ORCID ProfileMatthew C. Curtis, View ORCID ProfileLove Dalén, View ORCID ProfileMarta Díaz-Zorita Bonilla, View ORCID ProfileJ. Carlos Díez Fernández-Lomana, Dorothée G. Drucker, Elena Escribano Escrivá, View ORCID ProfileMichael Francken, View ORCID ProfileVictoria E. Gibbon, View ORCID ProfileManuel R. González Morales, Ana Grande Mateu, Katerina Harvati, View ORCID ProfileAmanda G. Henry, View ORCID ProfileLouise Humphrey, View ORCID ProfileMario Menéndez, View ORCID ProfileDušan Mihailović, View ORCID ProfileMarco Peresani, Sofía Rodríguez Moroder, View ORCID ProfileMirjana Roksandic, View ORCID ProfileHélène Rougier, View ORCID ProfileSandra Sázelová, Jay T. Stock, View ORCID ProfileLawrence Guy Straus, View ORCID ProfileJiří Svoboda, View ORCID ProfileBarbara Teßmann, View ORCID ProfileMichael J. Walker, View ORCID ProfileRobert C. Power, View ORCID ProfileCecil M. Lewis, Krithivasan Sankaranarayanan, View ORCID ProfileKaterina Guschanski, View ORCID ProfileRichard W. Wrangham, View ORCID ProfileFloyd E. Dewhirst, Domingo C. Salazar-García, View ORCID ProfileJohannes Krause, View ORCID ProfileAlexander Herbig, and View ORCID ProfileChristina Warinner
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PNAS May 18, 2021 118 (20) e2021655118; https://doi.org/10.1073/pnas.2021655118
Edited by Robert R. Dunn, North Carolina State University, Raleigh, NC, and accepted by Editorial Board Member James F. O’Connell March 22, 2021 (received for review October 16, 2020)

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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.

Abstract
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.

dental calculusmicrobiomeNeanderthalprimatesalivary amylase
The oral cavity is colonized by one of the most diverse sets of microbial communities of the human body, currently estimated at over 600 prevalent taxa (1). Dental diseases, such as caries and periodontitis, remain health burdens in all human populations despite hygiene interventions (2, 3), and oral microbes are often implicated in extraoral inflammatory diseases (4, 5)