The evolution and changing ecology of the African hominid oral microbiome

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.

Genomic Analysis of 18th-Century Kazakh Individuals and Their Oral Microbiome

“…Kuygenzhar’s Tannerella strains were screened for possible virulence, antibiotic resistance, and glycosylation genes that were obtained from the literature [ 76 ] ( Table S10 ), along with ancient European and Mexican strains and the modern strains that were previously included in the phylogeny. Genes that were phenotypically associated to these functions may have endured differential selection pressures due to changes of environment in time and location, for instance the use of antibiotics and the change to a more sugar-rich diet [ 73 ]. All of the strains were mapped against the gene sequences and the resulting gene-by-gene coverage is shown in Figure S15 .…”

“…While the focus of our work was on T. forsythia , we additionally considered the other oral pathogens for which sufficient aDNA was recovered; T. denticola and P. gingivalis . To place these ancient bacterial genomes in a modern context, we selected published samples from both species with more than 1X of average depth [ 73 ]. SNP datasets for each bacterium were created considering only variant positions covered in more than 75% of the samples.…”

Landscape modification by Last Interglacial Neanderthals

“…While the butchering of large herbivores created a highly visible archaeological record in the Neumark-Nord landscape and at Neanderthal sites in general, nutritional studies strongly suggest that these hominins could not have survived on terrestrial game only: Plants must have played an important role in Neanderthal diets, providing carbohydrates and some of the required nutrients and calories ( 76 ). A range of recent studies suggest that starch-rich foods were already important before the split between the Neanderthal and modern human lineages and document consumption of a similarly wide range of plant species by Neanderthals across their geographical range ( 76 , 77 ). If, as the archaeozoological data suggest, Neanderthals were indeed present during most parts of the year in the Neumark-Nord area, supplementing their animal-based diets with plant foods would have been an important part of their subsistence activities.…”

Neutrophils Orchestrate the Periodontal Pocket

“…Discrimination between supragingival and subgingival biofilm in fossils of individuals without periodontitis is not possible and only partly feasible in living animals for technical reasons. The fact that no discrimination has been reported in studies on fossils and animals ( 33 , 58 ) strongly suggests that the examined biofilm was either supragingival or mixed, thus limiting the usefulness of these studies on oral microbiome concerning periodontitis.…”