Pathogens and host immunity in the ancient human oral cavity

Christina Warinner; João F Matias Rodrigues; Rounak Vyas; Christian Trachsel; Natallia Shved; Jonas Grossmann; Anita Radini; Y Hancock; Raul Y Tito; Sarah Fiddyment; Camilla Speller; Jessica Hendy; Sophy Charlton; Hans Ulrich Luder; Domingo C Salazar-García; Elisabeth Eppler; Roger Seiler; Lars H. Hansen; Jose Alfredo Samaniego Castruita; Simon Barkow-Oesterreicher; Kai Yik Teoh; Christian Kelstrup; Jesper Velgaard Olsen; Paolo Nanni; Toshihisa Kawai; Eske Willerslev; Christian von Mering; Cecil M Lewis; Matthew J Collins; M. Thomas P. Gilbert; Frank Rühli; Enrico Cappellini

doi:10.1038/ng.2906

Pathogens and host immunity in the ancient human oral cavity

Christina Warinner, João F Matias Rodrigues, Rounak Vyas, Christian Trachsel, Natallia Shved, Jonas Grossmann, Anita Radini, Y Hancock, Raul Y Tito, Sarah Fiddyment, Camilla Speller, Jessica Hendy, Sophy Charlton, Hans Ulrich Luder, Domingo C Salazar-García, Elisabeth Eppler, Roger Seiler, Lars H. Hansen, Jose Alfredo Samaniego Castruita, Simon Barkow-OesterreicherKai Yik Teoh, Christian Kelstrup, Jesper Velgaard Olsen, Paolo Nanni, Toshihisa Kawai, Eske Willerslev, Christian von Mering, Cecil M Lewis, Matthew J Collins, M. Thomas P. Gilbert, Frank Rühli, Enrico Cappellini

294 Citations (Scopus)

Abstract

Calcified dental plaque (dental calculus) preserves for millennia and entraps biomolecules from all domains of life and viruses. We report the first, to our knowledge, high-resolution taxonomic and protein functional characterization of the ancient oral microbiome and demonstrate that the oral cavity has long served as a reservoir for bacteria implicated in both local and systemic disease. We characterize (i) the ancient oral microbiome in a diseased state, (ii) 40 opportunistic pathogens, (iii) ancient human-associated putative antibiotic resistance genes, (iv) a genome reconstruction of the periodontal pathogen Tannerella forsythia, (v) 239 bacterial and 43 human proteins, allowing confirmation of a long-term association between host immune factors, 'red complex' pathogens and periodontal disease, and (vi) DNA sequences matching dietary sources. Directly datable and nearly ubiquitous, dental calculus permits the simultaneous investigation of pathogen activity, host immunity and diet, thereby extending direct investigation of common diseases into the human evolutionary past.

Original language	English
Journal	Nature Genetics
Volume	46
Pages (from-to)	336-344
Number of pages	9
DOIs	https://doi.org/10.1038/ng.2906
Publication status	Published - Apr 2014

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Warinner, C., Rodrigues, J. F. M., Vyas, R., Trachsel, C., Shved, N., Grossmann, J., Radini, A., Hancock, Y., Tito, R. Y., Fiddyment, S., Speller, C., Hendy, J., Charlton, S., Luder, H. U., Salazar-García, D. C., Eppler, E., Seiler, R., Hansen, L. H., Samaniego Castruita, J. A., ... Cappellini, E. (2014). Pathogens and host immunity in the ancient human oral cavity. Nature Genetics, 46, 336-344. https://doi.org/10.1038/ng.2906

Warinner, C, Rodrigues, JFM, Vyas, R, Trachsel, C, Shved, N, Grossmann, J, Radini, A, Hancock, Y, Tito, RY, Fiddyment, S, Speller, C, Hendy, J, Charlton, S, Luder, HU, Salazar-García, DC, Eppler, E, Seiler, R, Hansen, LH, Samaniego Castruita, JA, Barkow-Oesterreicher, S, Teoh, KY, Kelstrup, C, Olsen, JV, Nanni, P, Kawai, T, Willerslev, E, von Mering, C, Lewis, CM, Collins, MJ, Gilbert, MTP, Rühli, F & Cappellini, E 2014, 'Pathogens and host immunity in the ancient human oral cavity', Nature Genetics, vol. 46, pp. 336-344. https://doi.org/10.1038/ng.2906

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title = "Pathogens and host immunity in the ancient human oral cavity",

abstract = "Calcified dental plaque (dental calculus) preserves for millennia and entraps biomolecules from all domains of life and viruses. We report the first, to our knowledge, high-resolution taxonomic and protein functional characterization of the ancient oral microbiome and demonstrate that the oral cavity has long served as a reservoir for bacteria implicated in both local and systemic disease. We characterize (i) the ancient oral microbiome in a diseased state, (ii) 40 opportunistic pathogens, (iii) ancient human-associated putative antibiotic resistance genes, (iv) a genome reconstruction of the periodontal pathogen Tannerella forsythia, (v) 239 bacterial and 43 human proteins, allowing confirmation of a long-term association between host immune factors, 'red complex' pathogens and periodontal disease, and (vi) DNA sequences matching dietary sources. Directly datable and nearly ubiquitous, dental calculus permits the simultaneous investigation of pathogen activity, host immunity and diet, thereby extending direct investigation of common diseases into the human evolutionary past.",

author = "Christina Warinner and Rodrigues, {Jo{\~a}o F Matias} and Rounak Vyas and Christian Trachsel and Natallia Shved and Jonas Grossmann and Anita Radini and Y Hancock and Tito, {Raul Y} and Sarah Fiddyment and Camilla Speller and Jessica Hendy and Sophy Charlton and Luder, {Hans Ulrich} and Salazar-Garc{\'i}a, {Domingo C} and Elisabeth Eppler and Roger Seiler and Hansen, {Lars H.} and {Samaniego Castruita}, {Jose Alfredo} and Simon Barkow-Oesterreicher and Teoh, {Kai Yik} and Christian Kelstrup and Olsen, {Jesper Velgaard} and Paolo Nanni and Toshihisa Kawai and Eske Willerslev and {von Mering}, Christian and Lewis, {Cecil M} and Collins, {Matthew J} and Gilbert, {M. Thomas P.} and Frank R{\"u}hli and Enrico Cappellini",

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AU - Grossmann, Jonas

AU - Radini, Anita

AU - Hancock, Y

AU - Tito, Raul Y

AU - Fiddyment, Sarah

AU - Speller, Camilla

AU - Hendy, Jessica

AU - Charlton, Sophy

AU - Luder, Hans Ulrich

AU - Salazar-García, Domingo C

AU - Eppler, Elisabeth

AU - Seiler, Roger

AU - Hansen, Lars H.

AU - Samaniego Castruita, Jose Alfredo

AU - Barkow-Oesterreicher, Simon

AU - Teoh, Kai Yik

AU - Kelstrup, Christian

AU - Olsen, Jesper Velgaard

AU - Nanni, Paolo

AU - Kawai, Toshihisa

AU - Willerslev, Eske

AU - von Mering, Christian

AU - Lewis, Cecil M

AU - Collins, Matthew J

AU - Gilbert, M. Thomas P.

AU - Rühli, Frank

AU - Cappellini, Enrico

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AB - Calcified dental plaque (dental calculus) preserves for millennia and entraps biomolecules from all domains of life and viruses. We report the first, to our knowledge, high-resolution taxonomic and protein functional characterization of the ancient oral microbiome and demonstrate that the oral cavity has long served as a reservoir for bacteria implicated in both local and systemic disease. We characterize (i) the ancient oral microbiome in a diseased state, (ii) 40 opportunistic pathogens, (iii) ancient human-associated putative antibiotic resistance genes, (iv) a genome reconstruction of the periodontal pathogen Tannerella forsythia, (v) 239 bacterial and 43 human proteins, allowing confirmation of a long-term association between host immune factors, 'red complex' pathogens and periodontal disease, and (vi) DNA sequences matching dietary sources. Directly datable and nearly ubiquitous, dental calculus permits the simultaneous investigation of pathogen activity, host immunity and diet, thereby extending direct investigation of common diseases into the human evolutionary past.

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JO - Nature Genetics

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Pathogens and host immunity in the ancient human oral cavity

Abstract

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