The evolution and changing ecology of the African hominid oral microbiome

James Fellows Yates , Irina Velsko , Franziska Aron , Cosimo Posth , Courtney Hofman , Rita Austin , Cody Parker , Allison Mann , Kathrin Nägele , Kathryn Weedman Arthur , John Arthur , Catherine Bauer , Isabelle Crevecoeur (1) , Christophe Cupillard (2) , Matthew Curtis , Love Dalén , Marta Díaz-Zorita Bonilla , J. Carlos Díez Fernández-Lomana , Dorothée Drucker , Elena Escribano Escrivá , Michael Francken , Victoria Gibbon , Manuel González Morales , Ana Grande Mateu , Katerina Harvati , Amanda Henry , Louise Humphrey , Mario Menéndez , Dušan Mihailović , Marco Peresani , Sofía Rodríguez Moroder , Mirjana Roksandic , Hélène Rougier , Sandra Sázelová , Jay Stock , Lawrence Guy Straus , Jiří Svoboda , Barbara Tessmann , Michael Walker , Robert Power , Cecil Lewis , Krithivasan Sankaranarayanan , Katerina Guschanski , Richard Wrangham , Floyd Dewhirst , Domingo Salazar-García , Johannes Krause , Alexander Herbig , Christina Warinner

1 PACEA - De la Préhistoire à l'Actuel : Culture, Environnement et Anthropologie
2 LCE - Laboratoire Chrono-environnement (UMR 6249)

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.

Domaines: Sciences de l'environnement

James Fellows Yates, Irina Velsko, Franziska Aron, Cosimo Posth, Courtney Hofman, et al.. The evolution and changing ecology of the African hominid oral microbiome. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118 (20), pp.e2021655118. ⟨10.1073/pnas.2021655118⟩. ⟨hal-03378217⟩