Scientists extract genetic secrets from 4,000-year-old teeth to illuminate the impact of changing human diets over the centuries
IMAGE:
KILLURAGH CAVE, IRELAND.
view moreCREDIT: CREDIT SAM MOORE, OWNER MARION DOWD.
Researchers at Trinity College Dublin have recovered remarkably preserved microbiomes from two teeth dating back 4,000 years, found in an Irish limestone cave. Genetic analyses of these microbiomes reveal major changes in the oral microenvironment from the Bronze Age to today. The teeth both belonged to the same male individual and also provided a snapshot of his oral health.
The study, carried out in collaboration with archaeologists from the Atlantic Technological University and University of Edinburgh, was published today in leading journal Molecular Biology and Evolution. The authors identified several bacteria linked to gum disease and provided the first high-quality ancient genome of Streptococcus mutans, the major culprit behind tooth decay.
While S. mutans is very common in modern mouths, it is exceptionally rare in the ancient genomic record. One reason for this may be the acid-producing nature of the species. This acid decays the tooth, but also destroys DNA and stops plaque from fossilising. While most ancient oral microbiomes are retrieved from fossilised plaque, this study targeted the tooth directly.
Another reason for the scarcity of S. mutans in ancient mouths may be the lack of favorable habitats for this sugar-loving species. An uptick of dental cavities is seen in the archaeological record after the adoption of cereal agriculture thousands of years ago, but a far more dramatic increase has occurred only in the past few hundred years when sugary foods were introduced to the masses.
The sampled teeth were part of a larger skeletal assemblage excavated from Killuragh Cave, County Limerick, by the late Peter Woodman of University College Cork. While other teeth in the cave showed advanced dental decay, no cavities were visible on the sampled teeth. However, one tooth produced an unprecedented amount of S. mutans DNA, a sign of an extreme imbalance in the oral microbial community.
“We were very surprised to see such a large abundance of S. mutans in this 4,000-year-old tooth,” said Dr Lara Cassidy, an assistant professor in Trinity’s School of Genetics and Microbiology, and senior author of the study. “It is a remarkably rare find and suggests this man was at a high risk of developing cavities right before his death.”
The researchers also found that other streptococcal species were virtually absent from the tooth. This indicates the natural balance of the oral biofilm had been upset – mutans had outcompeted the other streptococci leading to the pre-disease state.
The team also found evidence to support the "disappearing microbiome" hypothesis, which proposes modern microbiomes are less diverse than those of our ancestors. This is cause for concern, as biodiversity loss can impact human health. The two Bronze Age teeth produced highly divergent strains of Tannerella forsythia, a bacteria implicated in gum disease.
“These strains from a single ancient mouth were more genetically different from one another than any pair of modern strains in our dataset, despite the modern samples deriving from Europe, Japan and the USA,” explained Iseult Jackson, a PhD candidate at Trinity, and first author of the study. “This represents a major loss in diversity and one that we need to understand better.”
Very few full genomes from oral bacteria have been recovered prior to the Medieval era. By characterising prehistoric diversity, the authors were able to reveal dramatic changes in the oral microenvironment that have happened since.
Dr Cassidy added: “Over the last 750 years, a single lineage of T. forsythia has become dominant worldwide. This is the tell-tale sign of natural selection, where one strain rises rapidly in frequency due to some genetic advantage it holds over the others. T. forsythia strains from the industrial era onwards contain many new genes that help the bacteria colonise the mouth and cause disease.
“S. mutans has also undergone recent lineage expansions and changes in gene content related to pathogenicity. These coincide with humanity’s mass consumption of sugar, although we did find that modern S. mutans populations have remained more diverse, with deep splits in the S. mutans evolutionary tree pre-dating the Killuragh genome.”
The scientists believe this is driven by differences in the evolutionary mechanisms that shape genome diversity in these species.
“S. mutans is very adept at swapping genetic material between strains,” said Dr Cassidy. “This means an advantageous innovation can be spread across S. mutans lineages like a new piece of tech. This ability to easily share innovations may explain why this species retains many diverse lineages without one becoming dominant and replacing all the others.”
In effect, both these disease-causing bacteria have changed dramatically from the Bronze Age to today, but it appears that very recent cultural transitions in the industrial era have had an inordinate impact.
An EXAMPLE of a tooth prior to ancient DNA sampling. Note this was not the tooth sampled in the study.
CREDIT
Dr Lara Cassidy, Trinity.
JOURNAL
Molecular Biology and Evolution
What Bronze Age teeth say about the evolution of the human diet
OXFORD UNIVERSITY PRESS USA
IMAGE:
KILLURAGH CAVE, COUNTY LIMERICK, IRELAND.
view moreCREDIT: SAM MOORE AND MARION DOWD/MOLECULAR BIOLOGY AND EVOLUTION
A new paper in Molecular Biology and Evolution, published by Oxford Univeristy Press, uncovers well-preserved microbiomes from two 4,000 year old teeth in a limestone cave in Ireland. These contained bacteria that cause gum disease, as well as the first high quality ancient genome from S. mutans, an oral bacterium that is one of the major causes of tooth decay.
These discoveries allowed the researchers to assess the impact of past dietary changes on the oral microbiome across millennia, including major changes coinciding with the popularization of sugar and industrialization. The teeth, both derived from the same Bronze Age man, also provided a snapshot of oral health in the past, with one tooth showing evidence of microbiome dysbiosis.
Microbial DNA extracted from ancient human teeth can provide information on the evolution of the oral microbiome. How did our ancestors’ mouths differ from our own and why? The excellent preservation of DNA in fossilized dental plaque has made the oral cavity one of the best studied aspects of the ancient human body. However, scientists have retrieved very few full genomes from oral bacteria from prior to the Medieval era. Researchers have limited knowledge about prehistoric bacterial diversity and the relative impact of recent dietary changes compared to ancient ones, such as the spread of farming starting about ten thousand years ago.
S. mutans is the primary cause of dental cavities and very common in oral microbiomes. However, it is exceptionally rare in the ancient genomic record. One reason for its rarity could be its acid-producing nature – this acid causes the tooth to decay but also degrades DNA and prevents plaque from mineralizing. The absence of S. mutans DNA in ancient mouths could also reflect less favorable habitats for the species across most of human history. Archaeologists have observed an uptick in dental cavities in skeletal remains following the adoption of cereal agriculture, but cavities become much more common in the Early Modern period, beginning about 1500 AD.
The sampled teeth were among a large assemblage of skeletal remains excavated from a limestone cave at Killuragh, County Limerick, by the late Peter Woodman of University College Cork. While other teeth in the cave showed advanced dental decay there was no evidence of caries on the sampled teeth. Nevertheless, one tooth root yielded an unprecedented quantity of mutans sequences.
“We were very surprised to see such a large abundance of mutans in this 4,000 year old tooth” said Lara Cassidy, an assistant professor at Trinity College Dublin and senior author of the study. “It is a remarkably rare find and suggests this man was at high risk of developing cavities right before his death.”
The cool, dry, and alkaline conditions of the cave may have contributed to the exceptional preservation of S. mutans DNA, but its high abundance also points to dysbiosis. The researchers found that while S. mutans DNA was plentiful, other streptococcal species were virtually absent from the tooth sample. This implies that the natural balance of the oral biofilm had been upset – mutans had outcompeted the other species leading to a pre-disease state.
The study lends support to the “disappearing microbiome” hypothesis, which proposes the microbiomes of our ancestors were more diverse than our own today. Alongside the S. mutans genome, the authors reconstructed two genomes for T. forsythia – a bacteria involved in gum disease – and found them to be highly divergent from one another, implying much higher levels of strain diversity in prehistoric populations.
“The two sampled teeth contained quite divergent strains of T. forsythia” explained Iseult Jackson, a PhD candidate and first author of the study. “These strains from a single ancient mouth were more genetically different from one another than any pair of modern strains in our dataset, despite these modern samples deriving from Europe, Japan, and the USA. This is interesting because a loss of biodiversity can have negative impacts on the oral environment and human health.”
The reconstructed T. forsythia and S. mutans genomes revealed dramatic changes in the oral microenvironment over the last 750 years. In recent centuries, one lineage of T. forsythia has become dominant in global populations. This is the tell-tale sign of a selective episode – where one strain rises rapidly in frequency due to some genetic advantage. The researchers found that post-industrial T. forsythia genomes have acquired many new genes that help the bacteria colonize the oral environment and cause disease.
S. mutans also showed evidence of recent lineage expansions and changes in gene content, which coincide with the popularization of sugar. However, the investigators found that modern S. mutans populations have remained more diverse than T. forsythia, with deep splits in the mutans evolutionary tree pre-dating the Killuragh genome. They believe this is driven by differences in the evolutionary mechanisms that shape genome diversity in these species.
“S. mutans is very adept at swapping genetic material across strains.” said Cassidy “This allows an advantageous innovation to be spread across mutans lineages, rather than one lineage becoming dominant and replacing all others.”
In effect, both these disease-causing bacteria have changed dramatically from the Bronze Age to today, but it appears that very recent cultural transitions, such as the consumption of sugar, have had an inordinate impact.
The paper, “Ancient genomes from Bronze Age remains reveal deep diversity and recent adaptive episodes for human oral pathobionts,” is available (at midnight on March 27th) at https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msae017.
Direct correspondence to:
Lara Cassidy
Smurfit Institute of Genetics
Trinity College Dublin
Dublin 2, IRELAND
cassidl4@tcd.ie
To request a copy of the study, please contact:
Daniel Luzer
daniel.luzer@oup.com
JOURNAL
Molecular Biology and Evolution
METHOD OF RESEARCH
Content analysis
SUBJECT OF RESEARCH
People
ARTICLE TITLE
Ancient genomes from Bronze Age remains reveal deep diversity and recent adaptive episodes for human oral pathobionts
ARTICLE PUBLICATION DATE
27-Mar-2024
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