Evolution and Ecology of the Oral Microbiome

The oral microbiome is the second largest human-associated microbial community, after the gut, and oral microbes exhibit an astounding diversity of predicted protein functions compared with other body sites. Focusing on a diverse set of archaeological dental calculus samples, this project seeks to reconstruct the evolutionary history of the human oral microbiome by tracing major taxonomic and functional shifts in the hominid lineage.

Dental calculus deposits ca. 1100 CE.

The oral microbiome, and dental plaque in particular, holds a special place in the history of microbiology. The first undisputed description of bacteria appears in a letter written by Antoni van Leeuwenhoek to the Royal Society of London in 1683 in which he describes “very many small living Animals, which moved themselves very extravagantly” within his dental plaque. Attempting in vain to count them, he noted, ‘The number of these animals in the scurf of mans [sic] Teeth, are so many that I believe they exceed the number of Men in a kingdom.’ Van Leeuwenhoek’s analogy is, if anything, understated. The average healthy person carries on the surface of their teeth nearly as many bacteria as there are humans on the Earth, and every day each of us swallows an average of 80 billion bacteria in our saliva. The human oral cavity is thus more than a kingdom, it is an entire world unto itself.

Focusing on a diverse set of archaeological dental calculus samples, this project seeks to reconstruct the evolutionary history of the human oral microbiome by tracing major taxonomic and functional shifts in the hominid lineage. This project is run in collaboration with the Oral Microbiome Evolution Consortium (OMEC). See also: MPI-SHH Oral Microbiome Project page

Related Publications

Dental calculus collection.

Fellows Yates J, Velsko I, Aron F, Hofman C, Austin R, Arthur J, Crevecoeur I, Dalén L, Gonzalez Morales M, Guschanski K, Henry AG, Humphrey LT, Mann AE, Nägele K, Parker CE, Posth C, Rougier H, Semal P, Stock J, Guy Strauss L, Weedman Arthur K, Wrangham R, Curtis M, Diez JC, Gibbon V, Menedez M, Peresani M, Roksandic M, Walker MJ, Power RC, Lewis CM, Sankaranarayan K, Salazar-Garcia DC, Krause J, Herbig A, Warinner C. The evolution and changing ecology of the African hominid oral microbiome. PNAS 118 (20) e2021655118. https://doi.org/10.1073/pnas.2021655118

Fagernäs Z, Garcia Collado MI, Hendy J, Hofman C, Speller C, Velsko I, Warinner C. (2020) A unified protocol for simultaneous extraction of DNA and proteins from archaeological dental calculus. Journal of Archaeological Science 118:105135. https://doi.org/10.1016/j.jas.2020.105135

Velsko IM, Fellows-Yates JA, Aron F, Hagen RW, Frantz LAF, Loe L, Rodriguez Martinez JB, Chaves E, Gosden C, Larson G, Warinner C*. (2019) Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage. Microbiome 7:102. DOI: 10.1186/s40168-019-0717-3

Hofman CA, Warinner C*. (2019) Ancient DNA 101: An introductory guide in the era of high-throughput sequencing. SAA Record 19(1): 18-25.

Ziesemer KA, Ramos-Madrigal J, Mann AE, Brandt B, Sankaranarayanan K, Ozga A, Hoogland M, Salazar Garcia D, Frohlich B, Milner G, Aldenderfer M, Lewis CM, Hofman C, Warinner C, Schroeder H*. (2018) The efficacy of whole human genome and high-throughput sequencing on ancient dental calculus. American Journal of Physical Anthropology. DOI: 10.1002/ajpa.23763.

Velsko IM, Frantz LAF, Herbig A, Larson G, Warinner C*. (2018) Selection of appropriate metagenome taxonomic classifiers for ancient microbiome research. mSystems 3:e00080-18. DOI: 10.1128/mSystems.00080-18.

Mann AE, Sabin S, Ziesemer KA, Vågene Å, Schroeder H, Ozga A, Sankaranarayanan K, Hofman CA†, Fellows-Yates J, Salazar Garcia D, Frohlich B, Aldenderfer M, Hoogland M, Read C, Krause J, Hofman C, Bos K, Warinner C. (2018) Differential preservation of endogenous human and microbial DNA in dental calculus and dentin. Scientific Reports 8:9822.

Velsko IM, Overmyer KA, Speller C, Loe L, Sankaranarayanan K, Collins M, Lewis CM, Bautista Rodriguez J, Chaves E, Coon JJ, Larson G, Warinner C*. (2017) The dental calculus metabolome in modern and historic samples. Metabolomics 13:134

Warinner C, Herbig A, Mann AE, Fellows Yates JA, Weiss CL, Burbano HA, Orlando L, Krause J. (2017) A robust framework for microbial archaeology. Annu. Rev. Genom. Hum. Genet. 18:321-356.

Velsko I, Warinner C*. (2017) Bioarchaeology of the human microbiome. Bioarchaeology International 1(1-2):86-99. See also open access version.

Schnorr S, Sankaranarayanan K, Lewis CM, Warinner C*. (2016) Insights into human evolution from ancient and contemporary microbiome studies. Current Opinion in Genetics and Development 41:14-26.

Warinner C. (2016) Dental calculus and the evolution of the human oral microbiome. California Dental Association Journal 44(7):411-420.

Ozga AT, Nieves-Colón MA, Honap T, Sankaranarayanan K, Hofman C, Milner G, Lewis CM, Stone AC, Warinner C*. (2016) Successful enrichment and recovery of whole mitochondrial genomes from ancient human dental calculus. American Journal of Physical Anthropology 160:220-228.

Ziesemer KA, Mann AE, Sankaranarayanan K, Schroeder H, Ozga AT, Brandt BW, Zaura E, Waters-Rist A, Hoogland M, Salazar Garcia DC, Aldenderfer M, Speller C, Hendy J, Weston DA, MacDonald SJ, Thomas GH, Collins MJ, Lewis CM, Hofman C, Warinner C*. (2015) Intrinsic challenges in ancient microbiome reconstruction using 16S rRNA gene amplification. Scientific Reports 5, 16498. doi: 10.1038/srep16498.

Gram stain of ancient dental calculus.

Warinner C, Speller C, Collins MJ, Lewis CM* (2015) Ancient Human Microbiomes. Journal of Human Evolution 79, 125-136. http://dx.doi.org/10.1016/j.jhevol.2014.10.016

Warinner C*, Speller C, Collins MJ (2014) A New Era in Paleomicrobiology: Prospects for Ancient Dental Calculus as a Long-Term Record of the Human Oral Microbiome. Philosophical Transactions of the Royal Society B 370: 20130376. http://dx.doi.org/10.1098/rstb.2013.0376

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 L, Samaniego Castruita JA, Barkow-Oesterreicher S, Teoh KY, Kelstrup C, Olsen JV, Nanni P, Kawai T, Willerslev E, von Mering C, Lewis, Jr. CM, Collins MJ, Gilbert MTP, Rühli F, Cappellini E* (2014). Pathogens and host immunity in the ancient human oral cavity. Nature Genetics 46(4):336-344. doi:10.1038/ng.2906.

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