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

Abigail Gancz; Andrew Ferrer; Michelle Nixon; Stirling Wright; Luis Arriola; Adler Christina; Emily Davenport; Neville Gully; Alan Cooper; Kate Britton; Keith Dobney; Justin Silverman; Laura Weyrich

doi:10.1038/s41564-023-01527-3

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

Abigail Gancz, Andrew Ferrer, Michelle Nixon, Stirling Wright, Luis Arriola, Adler Christina, Emily Davenport, Neville Gully, Alan Cooper, Kate Britton, Keith Dobney, Justin Silverman, Laura Weyrich^* (Corresponding Author)

^*Corresponding author for this work

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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.

Original language	English
Pages (from-to)	2315-2325
Number of pages	11
Journal	Nature Microbiology
Volume	8
Early online date	29 Nov 2023
DOIs	https://doi.org/10.1038/s41564-023-01527-3
Publication status	Published - Dec 2023

Bibliographical note

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.

Data Availability Statement

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.

Keywords

dental diseases
evolutionary genetics
microbiome
ancient DNA
dental calculus
oral microbiome
Britain
London

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Data from: Ancient dental calculus reveals oral microbiome shifts associated with lifestyle and disease in Great Britain
Gancz, A. (Creator), Farrer, A. (Creator), Nixon, M. (Creator), Wright, S. (Creator), Arriola, L. (Creator), Christina, A. (Creator), Davenport, E. (Creator), Gully, N. (Creator), Cooper, A. (Creator), Britton, K. (Creator), Dobney, K. (Creator), Silverman, J. (Creator) & Weyrich, L. S. (Creator), University of Aberdeen, Nov 2023
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Cite this

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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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note = "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. ",

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doi = "10.1038/s41564-023-01527-3",

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AU - Nixon, Michelle

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AU - Arriola, Luis

AU - Christina, Adler

AU - Davenport, Emily

AU - Gully, Neville

AU - Cooper, Alan

AU - Britton, Kate

AU - Dobney, Keith

AU - Silverman, Justin

AU - Weyrich, Laura

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JO - Nature Microbiology

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ER -

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

Abstract

Bibliographical note

Data Availability Statement

Keywords

UN SDGs

Access to Document

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

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