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Ancient dental calculus reveals oral microbiome shifts associated with lifestyle and disease in Great Britain

Nature Microbiology volume 8, pages 2315–2325 (2023)Cite this article

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Abstract

The prevalence of chronic, non-communicable diseases has risen sharply in recent decades, especially in industrialized countries. While several studies implicate the microbiome in this trend, few have examined the evolutionary history of industrialized microbiomes. Here we sampled 235 ancient dental calculus samples from individuals living in Great Britain (∼2200 bce to 1853 ce), including 127 well-contextualized London adults. We reconstructed their microbial history spanning the transition to industrialization. After controlling for oral geography and technical biases, we identified multiple oral microbial communities that coexisted in Britain for millennia, including a community associated with Methanobrevibacter, an anaerobic Archaea not commonly prevalent in the oral microbiome of modern industrialized societies. Calculus analysis suggests that oral hygiene contributed to oral microbiome composition, while microbial functions reflected past differences in diet, specifically in dairy and carbohydrate consumption. In London samples, Methanobrevibacter-associated microbial communities are linked with skeletal markers of systemic diseases (for example, periostitis and joint pathologies), and their disappearance is consistent with temporal shifts, including the arrival of the Second Plague Pandemic. This suggests pre-industrialized microbiomes were more diverse than previously recognized, enhancing our understanding of chronic, non-communicable disease origins in industrialized populations.

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Fig. 1: Geographical and temporal distribution of samples.
Fig. 2: Oral geography and microbial compositions.
Fig. 3: Exploration of dominant taxa and communities.
Fig. 4: Abundance of dietary microbial functions in ancient Britain.

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Data availability

All trimmed and merged DNA sequences (fastq) are available in the SRA database (BioProject PRJNA780005) of NCBI. The 2017 NCBI nr database and the 2017 NCBI RefSeq GCS database were used in this study. Unmerged reads can be made available upon request, as only merged sequences were assessed in full for this publication.

Code availability

The analysis pipelines are available in the microARCH GitHub page (@microARCHlab/BritishDentalCalculus_2021), as well as in https://github.com/michellepistner/ancientDNA.

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Acknowledgements

We thank C. Stringer and R. Kruszynski of the Natural History Museum, London; S. Schiffels; D. Sayer; Oxford Archaeology East; M. Farrell of the Royal College of Surgeons of England; J. Pearson of the Inverness Museum; and all of the museums for access to samples. We also thank the Museum of London for allowing us to collect and destructively analyse archaeological dental calculus samples from their collections from London, particularly J. Bekvalac and R. Redfern. We would also like to acknowledge J. VanderBerg at EnDev Geographic for producing the map used in Fig. 1. A.C., C.A. and L.W. thank the Australian Research Council for research funding (DP110105038) and Laureate (FL140100260). The work was also supported by an Australian Research Council Future Fellowship Award to L.S.W. (FT180100407). This material is also based on work supported by the National Science Foundation Graduate Research Fellowship Program awarded to A.S.G. under Grant No. DGE1255832. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Author information

Author notes

  1. These authors contributed equally: Abigail S. Gancz, Andrew G. Farrer.

Authors and Affiliations

  1. Department of Anthropology, The Pennsylvania State University, State College, PA, USA

    Abigail S. Gancz, Sterling Wright & Laura S. Weyrich

  2. School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia

    Andrew G. Farrer, Luis Arriola, Alan Cooper & Laura S. Weyrich

  3. College of Information Sciences and Technology, The Pennsylvania State University, State College, PA, USA

    Michelle P. Nixon & Justin D. Silverman

  4. School of Medical Sciences, Faculty of Medicine and Health, The University of Sydney, Sydney, New South Wales, Australia

    Christina Adler

  5. Charles Perkins Centre, The University of Sydney, Sydney, New South Wales, Australia

    Christina Adler

  6. Department of Biology, The Pennsylvania State University, State College, PA, USA

    Emily R. Davenport

  7. Huck Institutes of the Life Sciences, The Pennsylvania State University, State College, PA, USA

    Emily R. Davenport & Laura S. Weyrich

  8. Institute for Computational and Data Sciences, The Pennsylvania State University, State College, PA, USA

    Emily R. Davenport & Justin D. Silverman

  9. School of Dentistry, Faculty of Health Sciences, University of Adelaide, Adelaide, South Australia, Australia

    Neville Gully

  10. Gulbali Institute, Charles Sturt University, Albury, New South Wales, Australia

    Alan Cooper

  11. Department of Archaeology, School of Geosciences, University of Aberdeen, Aberdeen, UK

    Kate Britton & Keith Dobney

  12. Department of Archaeology, Faculty of Arts and Social Sciences, University of Sydney, Sydney, New South Wales, Australia

    Keith Dobney

  13. Department of Archaeology, Classics and Egyptology, School of Histories, Languages and Cultures, University of Liverpool, Liverpool, UK

    Keith Dobney

  14. Department of Archaeology, Faculty of Environment, Simon Fraser University, Burnaby, British Columbia, Canada

    Keith Dobney

  15. Department of Statistics, The Pennsylvania State University, State College, PA, USA

    Justin D. Silverman

  16. Department of Medicine, The Pennsylvania State University, Hershey, PA, USA

    Justin D. Silverman

Authors
  1. Abigail S. Gancz
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Contributions

A.G.F., N.G., A.C., K.D. and L.S.W. conceived of the study and developed the experimental design. A.C., A.G.F., C.A., K.B., K.D. and L.S.W. worked on sample acquisition. A.G.F. completed the laboratory analysis. A.S.G., A.G.F., S.W. and L.A. completed the bioinformatics and computational analysis. A.S.G., M.P.N., E.R.D., J.D.S. and L.S.W. performed the statistical analysis. A.S.G., A.G.F. and L.S.W. wrote the paper, and all authors edited and commented on the paper.

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Correspondence to Laura S. Weyrich.

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Gancz, A.S., Farrer, A.G., Nixon, M.P. et al. Ancient dental calculus reveals oral microbiome shifts associated with lifestyle and disease in Great Britain. Nat Microbiol 8, 2315–2325 (2023). https://doi.org/10.1038/s41564-023-01527-3

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