Pathogens and host immunity in the ancient human oral cavity
Open accessAbstract
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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Viral and fungal taxa, as well as disease-associated microorganisms of the respiratory tract, have been identified both in ancient biofilms and in more recently mineralized biofilms.
“Viral and fungal taxa, as well as disease-associated microorganisms of the respiratory tract, have been identified both in ancient biofilms and in more recently mineralized biofilms (56).”
From Dental calculus: the calcified biofilm and its role in disease development (2018) · cites this paper as [56]
The Ancient Oral Microbiome section reports viral and fungal DNA in ancient dental calculus, and Carriage of Specific Pathogens identifies organisms implicated in respiratory illness there. The paper compares ancient calculus with modern controls, but the cited passages do not establish that all three groups were identified in more recently mineralized biofilms. (LLM, conf=0.86)
Experimental — accuracy not yet measuredDifferent metagenomic sequencing strategies have recently been applied to ancient dental calculus and described immense possibilities for dental calculus to reform ancient biomedical research.
“Different metagenomic sequencing strategies have recently been applied to ancient dental calculus and described immense possibilities for dental calculus to reform ancient biomedical research (56).”
From Dental calculus: the calcified biofilm and its role in disease development (2018) · cites this paper as [56]
The oral cavity is an ecological reservoir for potential pathogens and is involved in local and systemic diseases.
“it is supposed that the oral cavity, an ecological reservoir for potential pathogens, is involved in local and systemic diseases (Warinner et al., 2014).”
From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Warinner et al., 2014
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Zheng, Y., Ke, L., Lu, Y., Zuo, Q., Deng, G., Wang, H., & Zeng, X. (2020) · Frontiers in Chemistry · doi:10.3389/fchem.2020.00273 · Cited by 11 · see citing works
Santiago-Rodriguez, T. M., Fornaciari, A., Fornaciari, G., Luciani, S., Marota, I., Vercellotti, G., Toranzos, G. A., Giuffra, V., & Cano, R. J. (2019) · Genes · doi:10.3390/genes10040299 · Cited by 10 · see citing works
- Authors
- 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., Castruita, J. A. S., Barkow-Oesterreicher, S., Teoh, K. Y., Kelstrup, C. D., Olsen, J. V., Nanni, P., Kawai, T., Willerslev, E., von Mering, C., Lewis, C. M., Collins, M. J., Gilbert, M. T. P., Rühli, F., & Cappellini, E.
- Affiliations
- University of Zurich (CH)
- SIB Swiss Institute of Bioinformatics (CH)
- University of Leicester (GB)
- University of York (GB)
- University of Oklahoma (US)
- University of Copenhagen (DK)
- Harvard University (US)
- Corresponding author
- Warinner, Christina
- Cappellini, Enrico
- ORCID
- Warinner, Christina
- Rodrigues, João F Matias
- Trachsel, Christian
- Grossmann, Jonas
- Radini, Anita
- Hancock, Y
- Tito, Raul Y
- Fiddyment, Sarah
- Speller, Camilla
- Hendy, Jessica
- Charlton, Sophy
- Eppler, Elisabeth
- Seiler, Roger
- Hansen, Lars H
- Castruita, José Alfredo Samaniego
- Kelstrup, Christian D
- Olsen, Jesper V
- Nanni, Paolo
- Kawai, Toshihisa
- Willerslev, Eske
- von Mering, Christian
- Lewis, Cecil M
- Collins, Matthew J
- Gilbert, M Thomas P
- Rühli, Frank
- Cappellini, Enrico
- Venue
- Nature Genetics
- Published
- 2014-02-23
- Volume
- 46
- Issue
- 4
- Pages
- 336-344
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC3969750
- OpenAlex
- W2043470990
- Cited by
- 618
- References
- 74
- Citations by year
- 2026: 32 · 2025: 40 · 2024: 39 · 2023: 50 · 2022: 50 · 2021: 64 · 2020: 76 · 2019: 43 · 2018: 70 · 2017: 51 · 2016: 47 · 2015: 29 · 2014: 27
- FWCI
- 68.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc)
- Max Planck Digital Library (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Griffith Research Online (submittedVersion)
- Repository of Digital Objects for Teaching Research and Culture (University of Valencia) (submittedVersion, other-oa)
- Apollo (University of Cambridge) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Apollo
- Funders
- National Science Foundation
- Novartis Foundation
- Wellcome Trust (097829, 090207)
- European Commission (299075)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (135688, 29396, 31003A)
- Lundbeckfonden (R44-A4384, R109-2012-9995, R70-2010-6286, R155-2013-16338, R52‐A5062, R44-2009-4384, R38-2008-3048, R24-2008-2527)
- Max-Planck-Gesellschaft
- Novo Nordisk
- Danmarks Frie Forskningsfond (10‐081390)
- Novo Nordisk Fonden
- H. Lundbeck A/S
- Mäxi-Stiftung
- National Institutes of Health (5r01hg005172-03)
- Natural Environment Research Council (1219549)
- National Human Genome Research Institute (R01-HG005172)
- National Institute of General Medical Sciences (R01GM089886)
- National Institute of Dental and Craniofacial Research (R01DE018499, R21DE018310)
- FP7 People: Marie-Curie Actions (299101, FP7-PEOPLE-2011-IOF, FP7-PEOPLE-2011-IEF)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Social Sciences › Arts and Humanities › Archeology › Paleopathology and ancient diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
- Keywords
- periodontal disease, dental calculus, Tannerella forsythia, opportunistic pathogens, host immunity, antibiotic resistance genes, host-pathogen interaction, ancient human diet, paleomicrobiology
- MeSH terms
- Archaeology, Base Sequence, Dental Calculus, Food Analysis, Germany, Humans, Molecular Sequence Data, Mouth, Phylogeny, RNA, Ribosomal, 16S, Genome, Bacterial, Sequence Analysis, DNA, Proteome, Bacteroidetes, History, Medieval, Tandem Mass Spectrometry, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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