By the Skin of your Teeth: Investigating Chronic Periodontal Disease through History

Overview

Chronic periodontal disease is a very common chronic condition which includes the familiar gum disease but can spread to the other supportive tissues around the tooth, potentially resulting in bone deterioration and tooth loss.  The disease is caused by overgrowth of harmful bacteria in plaque and tartar deposits around the gum-line. Beyond its effects on oral health, individuals with chronic periodontitis are also at higher risk for cardiovascular disease, stroke, diabetes, and respiratory illnesses.

In order to effectively treat periodontal disease today, we need to have a clear understanding of both the species of bacterial pathogens that cause the disease in the past and today, and how these bacteria have evolved through time. Archaeological studies have known that humans have been suffering from periodontal disease for millennia, although frequency and severity vary between geographic areas and historical periods. This study will investigate the genetic diversity and evolution of periodontal pathogens from five historic time periods in Yorkshire through biomolecular analyses of fossilised plaque on human skull remains. It will also examine different human immune responses over time in order to learn more about the bacteria's virulence and adaptability.

The initial results of metagenomic analyses indicate that bacterial DNA is well preserved in dental calculus, and that DNA yields are sufficient to reconstruct ancient periodontal pathogen genomes. We have completed genome reconstructions for two periodontal pathogens, Tannerella forsythia and Treponema denticola, dating to the Medieval period. Both genomes are distinct from modern strains, as well as from medieval strains recovered from Germany. Our results confirm that, in general, dental calculus represents a robust substrate for investigating ancient oral microbiomes - we are in the process of documenting variation in oral microbial communities through time and space.

Camilla Speller presented an overview of the project to public audiences at the Archaeology Open Day at the Washburn Heritage Centre in Fewston, May 8, 2013. She gave a talk entitled "the Yorkshire Oral Microbiome Project: Then and Now" discussing the archaeological samples from Fewston included in the C2D2 project, and then potential of dental calculus to understand past health. Speller also gave an interview on BBC Radio York's Science program related to the research output "Pathogens and host immunity in the ancient human oral cavity".

Press Releases

• Scientists unlock a ‘microbial Pompeii’

In detail

Chronic periodontal disease is a very common chronic condition which includes the familiar gum disease but can spread to the other supportive tissues around the tooth, potentially resulting in bone deterioration and tooth loss.  The disease is caused by overgrowth of harmful bacteria in plaque and tartar deposits around the gum-line. Beyond its effects on oral health, individuals with chronic periodontitis are also at higher risk for cardiovascular disease, stroke, diabetes, and respiratory illnesses.

In order to effectively treat periodontal disease today, we need to have a clear understanding of both the species of bacterial pathogens that cause the disease in the past and today, and how these bacteria have evolved through time. Archaeological studies have known that humans have been suffering from periodontal disease for millennia, although frequency and severity vary between geographic areas and historical periods. This study will investigate the genetic diversity and evolution of periodontal pathogens from five historic time periods in Yorkshire through biomolecular analyses of fossilised plaque on human skull remains. It will also examine different human immune responses over time in order to learn more about the bacteria's virulence and adaptability.

Our analyses extracted and analyzed both proteins and DNA preserved in ancient dental calculus. The results of the proteomic analysis indicate that there is considerable variation in the preservation of proteins between individuals and time periods, and abundance of human vs bacterial proteins. In particular, our project uncovered the presence of beta-lactoglobulin (BLG), a dietary milk protein, in many of our archaeological samples. The presence of BLG in dental calculus represents a novel individual skeletal marker for dairy consumption, and has important implications for studying the emergence of dairying and the evolution of lactase persistence in the past. Based on this pilot data, we are expanding our dental calculus research to investigate the robustness and sensitivity of this milk-consumption marker in archaeological remains. We are also continuing to examine the correspondence between the biomolecular and skeletal indicators of periodontitis progression and severity.

The initial results of the metagenomic analyses indicate that bacterial DNA is well preserved in dental calculus, and that DNA yields are sufficient to reconstruct ancient periodontal pathogen genomes. We have completed genome reconstructions for two periodontal pathogens, Tannerella forsythia and Treponema denticola, dating to the Medieval period. Both genomes are distinct from modern strains, as well as from medieval strains recovered from Germany. Our amplicon metagenomic results confirm that, in general, dental calculus represents a robust substrate for investigating ancient oral microbiomes - we are in the process of documenting variation in oral microbial communities through time and space.

Prof Matthew Collins has been invited to speak about the project at National Trust Regional group York, the 41 Club, and the York ProBus club. He also presented preliminary results at the Association for Veterinary Teaching and Research Work meeting in April 2013. Dr. Camilla Speller was invited to present preliminary results at the NERC International Environmental ‘Omics Synthesis Conference in Cardiff, in September 2013 and gave a presentation at the C2D2 conference in Sept 2013 with Gavin Thomas (Co-I). Speller will also present the results of the project at a NERC sponsored Environmental Proteomics symposium in Sheffield, July 2, 2014.

Outputs

Publications

• 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. (2014) Pathogens and host immunity in the ancient human oral cavity. Nature Genetics, 46(4):336-44. doi: 10.1038/ng.2906.
• Warinner, C., Speller, C. F. & Collins, M. J. (2014). Paleomicrobiology of the Human Oral Microbiome. Philosophical Transactions of the Royal Society London B.
• Ziesemer, K. A., Mann, A. E., Sankaranarayanan, K., Schroeder, H., Ozga, A. T., Brandt, B. W., ... Warinner, C. (2015). Intrinsic challenges in ancient microbiome reconstruction using 16S rRNA gene amplification. Scientific Reports, 5, 1-19. doi: 10.1038/srep16498