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Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions

Nature Genetics volume 45, pages 450–455 (2013)Cite this article

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Abstract

The importance of commensal microbes for human health is increasingly recognized1,2,3,4,5, yet the impacts of evolutionary changes in human diet and culture on commensal microbiota remain almost unknown. Two of the greatest dietary shifts in human evolution involved the adoption of carbohydrate-rich Neolithic (farming) diets6,7 (beginning ∼10,000 years before the present6,8) and the more recent advent of industrially processed flour and sugar (in ∼1850)9. Here, we show that calcified dental plaque (dental calculus) on ancient teeth preserves a detailed genetic record throughout this period. Data from 34 early European skeletons indicate that the transition from hunter-gatherer to farming shifted the oral microbial community to a disease-associated configuration. The composition of oral microbiota remained unexpectedly constant between Neolithic and medieval times, after which (the now ubiquitous) cariogenic bacteria became dominant, apparently during the Industrial Revolution. Modern oral microbiotic ecosystems are markedly less diverse than historic populations, which might be contributing to chronic oral (and other) disease in postindustrial lifestyles.

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Figure 1: Phylum-level microbial composition of ancient dental calculus deposits.
Figure 2: Principal-components plot of β diversity.
Figure 3: Changes in the diversity and composition of oral microbiota.
Figure 4: Discriminant analysis of β diversity.

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Acknowledgements

We thank D. Brothwell for original inspiration, N. Gully and S. Bent for critical discussions and J. Soubrier for bioinformatics assistance. We thank H. Meller from the State Heritage Museum of Saxony-Anhalt, Germany, and W. Gumiński from the Institute of Archaeology, University of Warsaw, Poland, for prehistoric samples and members of the Australian Centre for Ancient DNA for practical help and providing samples of plaque and calculus. We thank several anonymous reviewers whose comments have considerably improved the manuscript. We thank the Australian Research Council, the Wellcome Trust (WT092799/Z/10/Z and WT098051) and the Sir Mark Mitchell Foundation for funding support.

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Authors and Affiliations

  1. Australian Centre for Ancient DNA, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, South Australia, Australia

    Christina J Adler, Laura S Weyrich, Wolfgang Haak & Alan Cooper

  2. Environment Institute, The University of Adelaide, Adelaide, South Australia, Australia

    Christina J Adler, Laura S Weyrich, Wolfgang Haak, Corey J A Bradshaw & Alan Cooper

  3. Institute of Dental Research, Westmead Millennium Institute, Faculty of Dentistry, University of Sydney, Sydney, New South Wales, Australia

    Christina J Adler

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

    Keith Dobney

  5. School of Dentistry, The University of Adelaide, Adelaide, South Australia, Australia

    John Kaidonis & Grant Townsend

  6. The Wellcome Trust Sanger Institute, Hinxton, Cambridge, UK

    Alan W Walker & Julian Parkhill

  7. School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, South Australia, Australia

    Corey J A Bradshaw

  8. South Australian Research and Development Institute, Henley Beach, South Australia, Australia

    Corey J A Bradshaw

  9. Department of Bioarchaeology, Institute of Archaeology, University of Warsaw, Warsaw, Poland

    Arkadiusz Sołtysiak

  10. Institute for Anthropology, Johannes Gutenberg University of Mainz, Mainz, Germany

    Kurt W Alt

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Contributions

C.J.A., A.C., K.D., A.W.W., J.P., K.W.A., G.T., J.K. and W.H. designed the study. C.J.A., K.D., K.W.A., A.S., W.H., A.C. and J.K. collected samples. C.J.A. and L.S.W. extracted and amplified DNA from dental calculus. C.J.A. and L.S.W. analyzed sequence data. A.W.W. performed 454 sequencing. C.J.A.B. performed α diversity bootstrapping analyses. C.J.A., A.C. and K.D. wrote the manuscript. All authors discussed the results and contributed to writing the manuscript.

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Correspondence to Alan Cooper.

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Adler, C., Dobney, K., Weyrich, L. et al. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet 45, 450–455 (2013). https://doi.org/10.1038/ng.2536

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