Tracking the transition to agriculture in Southern Europe through ancient DNA analysis of dental calculus (original) (raw)
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Ancient oral microbiomes support gradual Neolithic dietary shifts towards agriculture
Nature Communications, 2022
The human microbiome has recently become a valuable source of information about host life and health. To date little is known about how it may have evolved during key phases along our history, such as the Neolithic transition towards agriculture. Here, we shed light on the evolution experienced by the oral microbiome during this transition, comparing Palaeolithic hunter-gatherers with Neolithic and Copper Age farmers that populated a same restricted area in Italy. We integrate the analysis of 76 dental calculus oral microbiomes with the dietary information derived from the identification of embedded plant remains. We detect a stronger deviation from the hunter-gatherer microbiome composition in the last part of the Neolithic, while to a lesser extent in the early phases of the transition. Our findings demonstrate that the introduction of agriculture affected hostmicrobiome, supporting the hypothesis of a gradual transition within the investigated populations
The field of palaeomicrobiology is dramatically expanding thanks to recent advances in high-throughput biomolecular sequencing, which allows unpre- cedented access to the evolutionary history and ecology of human-associated and environmental microbes. Recently, human dental calculus has been shown to be an abundant, nearly ubiquitous, and long-term reservoir of the ancient oral microbiome, preserving not only microbial and host biomolecules but also dietary and environmental debris. Modern investigations of native human microbiota have demonstrated that the human microbiome plays a central role in health and chronic disease, raising questions about changes in microbial ecology, diversity and function through time. This paper explores the current state of ancient oral microbiome research and discusses successful applications, methodological challenges and future possibilities in elucidating the intimate evolutionary relationship between humans and their microbes.
2021
The oral cavity is a heterogeneous environment, varying in factors such as pH, oxygen levels, and salivary flow. These factors affect the microbial community composition and distribution of species in dental plaque, but it is not known how well these patterns are reflected in archaeological dental calculus. In most archaeological studies, a single sample of dental calculus is studied per individual and is assumed to represent the entire oral cavity. However, it is not known if this sampling strategy introduces biases into studies of the ancient oral microbiome. Here, we present the results of a shotgun metagenomic study of a dense sampling of dental calculus from four Chalcolithic individuals from the southeast Iberian peninsula (ca. 4500-5000 BP). Inter-individual differences in microbial composition are found to be much larger than intra-individual differences, indicating that a single sample can indeed represent an individual in most cases. However, there are minor spatial patter...
We report a molecular methodology to obtain and analyse ancient bacterial DNA from archaeological dental calculus. Recent and archaeological DNA samples, as old as 4000 bp, were successfully extracted and amplified with species-specific PCR primers. We propose this approach in order to: detect the presence of specific bacterial species infecting past human populations; compare the composition of ancient oral microbiomes among human populations; and analyse the genetic variability and covariation of bacteria and human host populations. Genomic analysis of bacteria from dental calculus is a promising source of evidence for palaeopathological and micro-evolutionary studies, focused either on micro-organisms or their human hosts.
Biological and cultural drivers of oral microbiota in Medieval and Post-Medieval London, UK
The trillions of microorganisms that live in association with the human body (microbiota) are critical for human health and disease, but there is a limited understanding of how cultural and environmental factors shaped our microbiota diversity through time. However, biomolecular remnants of the human oral microbiota - recovered from the calcified dental plaque (calculus) of our long-dead ancestors - are providing a new means of exploring this key relationship of our evolutionary history. Here, we correlate extensive experimental, archaeological, and biological metadata with 128 ancient dental calculus specimens from Medieval and Post-Medieval London, UK (1066 – 1853 CE). We identify a significant association between microbiota and oral geography (i.e. tooth type and tooth surface), which has confounded ancient microbiota studies to date. By controlling for oral geography, however, we identify the first associations between ancient microbiota and cultural and environmental signatures...
The making of the oral microbiome in Agta hunter-gatherers
Ecological and genetic factors have influenced the composition of the human microbiome during our evolutionary history. We analyzed the oral microbiota of the Agta, a hunter-gatherer population where part of its members is adopting an agricultural diet. We show that age is the strongest factor modulating the microbiome, likely through immunosenescence as there is an increase of pathogenicity with age. Biological and cultural processes generate sexual dimorphism in the oral microbiome. A small subset of oral bacteria is influenced by the host genome, linking host collagen genes to bacterial biofilm formation. Our data also suggests that shifting from a fish/meat to a rice-rich diet transforms their microbiome, mirroring the Neolithic transition. All these factors have implications in the epidemiology of oral diseases. Thus, the human oral microbiome is multifactorial, and shaped by various ecological and social factors that modify the oral environment.
Genes
Recent advantages in paleomicrobiology have provided an opportunity to investigate the composition of ancient microbial ecologies. Here, using metagenome analysis, we investigated the microbial profiles of historic dental calculus retrieved from archaeological human remains from postmedieval Latvia dated 16–17th century AD and examined the associations of oral taxa and microbial diversity with specific characteristics. We evaluated the preservation of human oral microbiome patterns in historic samples and compared the microbial composition of historic dental calculus, modern human dental plaque, modern human dental calculus samples and burial soil microbiota. Overall, the results showed that the majority of microbial DNA in historic dental calculus originated from the oral microbiome with little impact of the burial environment. Good preservation of ancient DNA in historical dental calculus samples has provided reliable insight into the composition of the oral microbiome of postmedi...
Philosophical Transactions of the Royal Society B: Biological Sciences, 2020
Human microbiome studies are increasingly incorporating macroecological approaches, such as community assembly, network analysis and functional redundancy to more fully characterize the microbiome. Such analyses have not been applied to ancient human microbiomes, preventing insights into human microbiome evolution. We address this issue by analysing published ancient microbiome datasets: coprolites from Rio Zape ( n = 7; 700 CE Mexico) and historic dental calculus ( n = 44; 1770–1855 CE, UK), as well as two novel dental calculus datasets: Maya ( n = 7; 170 BCE-885 CE, Belize) and Nuragic Sardinians ( n = 11; 1400–850 BCE, Italy). Periodontitis-associated bacteria ( Treponema denticola , Fusobacterium nucleatum and Eubacterium saphenum ) were identified as keystone taxa in the dental calculus datasets. Coprolite keystone taxa included known short-chain fatty acid producers ( Eubacterium biforme, Phascolarctobacterium succinatutens ) and potentially disease-associated bacteria ( Esche...