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Ancient Oral Microbiomes Reveal Similarities Between Neanderthals, Modern Humans

NEW YORK – By reconstructing oral metagenomes from up to 100,000 years ago, an international team of researchers has found that the microbial profiles of Neanderthals and modern humans shared functional adaptations for nutrient metabolism.

In a study published on Monday in the Proceedings of the National Academy of Sciences, the researchers analyzed 124 dental biofilm metagenomes from Neanderthals, Late Pleistocene-era humans, modern humans, chimpanzees, gorillas, and New World howler monkeys in order to examine the global diversity, variation, and evolution of the oral microbiome.

They found that a core microbiome of structural taxa has been maintained throughout African hominid evolution, and that humans also share these microbial groups with howler monkeys, suggesting that they have been important oral components since before the catarrhine-platyrrhine split, about 40 million years ago.

However, their analyses also revealed that Neanderthal and modern human microbial profiles are highly similar, and share functional adaptations for nutrient metabolism. These include an acquisition of salivary amylase-binding capability by oral streptococci that was apparently Homo-specific, suggesting that microbes co-adapted with the host's diet.

Further, the researchers found evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that they didn't observe in later modern human populations, providing insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

"The results of our study really emphasized to me just how similar Neanderthals and modern humans are. It is not only their DNA that shows signatures of close interrelationships, but they also appear to have very similar microbiomes," first author James Fellows Yates, a PhD student in the department of archaeogenetics at the Max Planck Institute for the Science of Human History, wrote in an email. "This is in contrast to a lot of widespread belief that Neanderthals were quite different from us. I'm excited to see what more information can be gleaned from the analysis of Neanderthal microbiomes, given the ability of bacteria to evolve much faster than their hosts and their rapid adaptability to changes in host behavior and diet."

The researchers generated and analyzed eight dental calculus metagenomes from present-day modern humans, 29 from gorillas, 20 from chimpanzees, 13 from Neanderthals, five from howler monkeys, 20 from a group of pre-agricultural archaeological modern humans, and 14 from a group of pre-antibiotic archaeological modern humans. They also added previously published microbiome data from one chimpanzee, four Neanderthals, and 10 present-day modern humans to their dataset.

They tested whether the oral microbiomes of the hominids reflected host phylogeny, and found that African hominid oral microbiota were distinguished by major taxonomic and functional differences that only weakly reflected host relationships. Rather, these microbiomes were more likely influenced by other physiological, dietary, or behavioral factors, the researcher said.

Hierarchical clustering showed that calculus metagenomes tended to cluster by host genus, confirming intragroup similarity, but that these relationships exhibited differences from host phylogeny. For example, howler monkeys and gorillas fell together in a single clade, and a subset of Homo clustered with chimpanzees. Overall, gorillas and howler monkeys were characterized by a wide diversity of aerobic and facultatively anaerobic taxa, while chimpanzees had higher levels of obligately anaerobic taxa. Neanderthals consistently fell within the diversity of modern humans.

They also compared the microbial profiles of Neanderthals and modern humans and found a high consistency of oral microbiome structure within Homo, regardless of geography, time period, or diet and lifestyle. They specifically detected the persistence of shared genetic diversity in core taxa between Neanderthals and Upper Paleolithic humans prior to 14,000 years ago, which also suggested that there was earlier admixture and interaction between the two groups in Ice Age Europe than previously thought.

In one analysis, the researchers determined that Homo-specific shifts in oral biofilm are linked to the availability of dietary starch. The Streptococcus species they found present in Homo oral biofilm that weren't present in the chimpanzee and nonhuman primate samples are notable for their ability to express amylase-binding proteins to capture salivary ɑ-amylase, which they use for their own nutrient acquisition from dietary starch, as well as dental adhesion, the researchers said.

Alpha-amylase is the most abundant enzyme in modern human saliva and modern humans express it at higher levels than any other hominid. In contrast to most other nonhuman primates, modern humans exhibit high salivary ɑ-amylase (AMY1) copy number variation, and this copy number expansion is estimated to have occurred along the modern human lineage after we diverged from Neanderthals in the Middle Pleistocene. The prevailing hypothesis is that this increase is connected to an increased reliance on starch-rich foods in the evolutionary history of modern humans.

Other sources of ancient microbial DNA may also add to this analysis in future studies, though Fellows Yates noted that dental calculus is the best source of ancient microbiomes, given its intrinsic mineralized nature.

"Palaeofaeces are occasionally found in the archaeological record and have already been shown to preserve a remnant of the gut microbiome," he said. "Further exploration into mummies from cold environments, or preserved specimens in natural history museum collections may also find some potential sources of more recent ancient microbiomes (e.g. from preserved skins). But in both cases, these types of specimens are rare. Therefore, the vast majority of ancient microbiome results will come from mineralized biofilms such as dental calculus."