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, a multinational team of scientists analyzed dental biofilm metagenomes of Neanderthals and Late Pleistocene to present-day humans spanning the past 100,000 years and compared them with those of chimpanzees, gorillas, and New World howler monkeys. They found 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 a Homo-specific acquisition of starch digestion capability in oral Streptococcus bacteria.
“We were able to show that bacterial DNA from the oral microbiome preserves at least twice as long as previously thought,” said James Fellows Yates, a doctoral candidate at the Max Planck Institute for the Science of Human History.
“The tools and techniques developed in this study open up new opportunities for answering fundamental questions in microbial archaeology, and will allow the broader exploration of the intimate relationship between humans and their microbiome.”
“Using these new tools, we also reconstructed the 100,000-year-old oral microbiome of a Neanderthal from Pešturina Cave in Serbia, the oldest oral microbiome successfully reconstructed to date by more than 50,000 years.”
After applying their rigorous strategy to identify, decontaminate, and authenticate well-preserved dental specimens, the researchers identified a core group of 10 bacterial species within the African hominid primate oral microbiome that are also shared with howler monkeys.
The findings suggest that these core species have played a key role in oral biofilms for over 40 million years.
Today, they are primarily involved in providing structural support within the dental plaque biofilm, and their study holds promise for understanding biofilm growth and maturation in the ancestral human microbiome.
The authors identified 27 genus-level members of the Homo core oral microbiome, and these include many well-known and clinically relevant species, such as Streptococcus and the pathogens Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola.
However, nearly all of these are also core microbiome members of other African hominids.
Only Veillonella parvula, a commensal species known to have a synergistic relationship with the pathogen Streptococcus mutans, is primarily found in humans.
Surprisingly, not all members of the core Homo oral microbiome are well-known: three have no genus designation and several lack species names, revealing a major gap in oral microbiology research that in part relates to the difficulties in growing and propagating these microbes.
“That many of the most important taxa are poorly characterized is a surprise to oral microbiologists who have been working on these bugs for years,” said Dr. Floyd Dewhirst, a researcher at the Forsyth Institute.
“We’re still learning about new members of this community, and these results give us new species to target for full characterization.”
The team also found that ancient humans living in Ice Age Europe shared some bacterial strains with Neanderthals.
Because the oral microbiome is typically acquired in early childhood from caregivers, this sharing may reflect earlier human-Neanderthal pairings and child rearing.
Furthermore, the researchers also found that Neanderthal-like bacterial strains were no longer found in humans after 14,000 years ago, a period during which there was substantial population turnover in Europe at the end of the last Ice Age.
“Oral bacteria provide an unexpected opportunity for reconstructing the interactions of humans and Neanderthals tens of thousands of years ago,” said Dr. Irina Velsko, a postdoctoral researcher at the Max Planck Institute for the Science of Human History.
“The intersection of human and microbial evolutionary biology is fascinating.”
The scientists also found that a subgroup of Streptococcus bacteria present in both modern humans and Neanderthals appears to have specially adapted to consume starch early in Homo evolution.
This suggests that starchy foods became important in the human diet prior to the split between Neanderthal and modern human lineages more than 600,000 years ago.
“Reconstructing what was on the menu for our most ancient ancestors is a difficult challenge, but our oral bacteria may hold important clues for understanding the early dietary shifts that have made us uniquely human,” said Professor Christina Warinner, a researcher at Harvard University and the Max Planck Institute for the Science of Human History.
“Bacterial genomes evolve much more quickly than the human genome, making our microbiome a particularly sensitive indicator of major events in our distant and recent evolutionary past.”
The results appear in the Proceedings of the National Academy of Sciences.
James A. Fellows Yates et al. 2021. The evolution and changing ecology of the African hominid oral microbiome. PNAS 118 (20): e2021655118; doi: 10.1073/pnas.2021655118
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