Award Abstract # 1516633
Evolution and Ecology of the Human Oral Microbiome

NSF Org: BCS
Division of Behavioral and Cognitive Sciences
Recipient: UNIVERSITY OF OKLAHOMA
Initial Amendment Date: July 22, 2015
Latest Amendment Date: July 22, 2015
Award Number: 1516633
Award Instrument: Standard Grant
Program Manager: Rebecca Ferrell
rferrell@nsf.gov
 (703)292-7850
BCS
 Division of Behavioral and Cognitive Sciences
SBE
 Directorate for Social, Behavioral and Economic Sciences
Start Date: August 1, 2015
End Date: July 31, 2018 (Estimated)
Total Intended Award Amount: $101,487.00
Total Awarded Amount to Date: $101,487.00
Funds Obligated to Date: FY 2015 = $101,487.00
History of Investigator:
  • Christina Warinner (Principal Investigator)
    warinner@fas.harvard.edu
  • Cecil Lewis (Co-Principal Investigator)
Recipient Sponsored Research Office: University of Oklahoma Norman Campus
660 PARRINGTON OVAL RM 301
NORMAN
OK  US  73019-3003
(405)325-4757
Sponsor Congressional District: 04
Primary Place of Performance: University of Oklahoma Norman Campus
101 David L. Boren Blvd.
Norman
OK  US  73019-5300
Primary Place of Performance
Congressional District:
04
Unique Entity Identifier (UEI): EVTSTTLCEWS5
Parent UEI:
NSF Program(s): Biological Anthropology
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1392, 9150, 9178, 9179
Program Element Code(s): 139200
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.075

ABSTRACT

The human microbiome, the sum total of bacteria that live in and on the human body, harbors 90% of our cells and >99% of our genes, and plays a critical role in performing many basic human life functions. And yet, we know very little about its diversity, variation, and evolution. The human oral cavity alone harbors a complex ecosystem containing more than 1,000 microbial species, and this oral microbiome has been associated with tooth decay, cardiovascular disease and a range of respiratory illnesses. Recently it has been discovered that dental calculus (calcified dental plaque) entraps a rich record of the oral microbiome that preserves for thousands of years. The objective of this study is to use metagenomic and metaproteomic approaches to systematically characterize the oral microbiome of chimpanzees and humans from the Paleolithic to the present. This study will contribute to reconstructing the human oral microbiome through time and understanding the origins of common oral pathogens and diseases. Findings from this study will also contribute to student training, and public science outreach and education.

Few studies have conducted basic research on the natural variation of the human oral microbiome or on changes in the oral microbiome through time. As a result little is known about the origins and evolutionary ecology of the human oral microbiome. Recently it has been discovered that dental calculus (calcified dental plaque) entraps a rich biomolecular record of the oral microbiome that preserves for thousands of years. This project will use state-of-the-art metagenomic and metaproteomic technologies to characterize the microbes of the oral cavity collected from chimpanzees and extinct and extant members of Homo: archaic Homo heidelbergensis (ca. 430,000 BP), Paleolithic H. sapiens (ca. 23,000 BP and 20,000 BP), Chalcolithic H. sapiens (ca. 4,000 BP), and present-day humans and chimpanzees. These samples will provide a path to reconstructing the the human oral microbiome over the course of hominin evolution.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 20)
Hendy J, Warinner C, Barnes I, Bouwman A, Collins M, Fiddyment S, Fischer R, Hagan R, Hofman CA, Holst M, Chaves E, Klaus L, Larson G, Mackie M, McGrath K, Mundorff A, Radini A, Rao H, Trachsel C, Velsko I, Speller C "Proteomic evidence of dietary sources in ancient dental calculus" Proceedings of the Royal Society B , v.285 , 2018 , p.20180977 10.1098/rspb.2018.0977
Jessica Hendy, Frido Welker, Beatrice Demarchi, Camilla Speller, Christina Warinner, Matthew J. Collins "A Guide to Ancient Protein Studies" Nature Ecology and Evolution , 2018 10.1038/s41559-018-0510-x
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 "Differential preservation of endogenous human and microbial DNA in dental calculus and dentin" Scientific Reports , 2018 10.1038/s41598-018-28091-9
Morales-Arce AY, Hofman CA, Duggan A, Benfer A, Katzenberg MA, McCafferty G, Warinner C "Successful reconstruction of whole mitochondrial genomes from ancient Central America and Mexico" Scientific Reports , 2017 10.1038/s41598-017-18356-0
Ozga AT, Nieves-Colón MA, Honap T, Sankaranarayanan K, Hofman C, Milner G, Lewis CM, Stone AC, Warinner C "Successful enrichment and recovery of whole mitochondrial genomes from ancient human dental calculus" American Journal of Physical Anthropology , v.160 , 2015 10.1002/ajpa.22960
Ozga AT, Nieves-Colón MA, Honap T, Sankaranarayanan K, Hofman C, Milner G, Lewis CM, Stone AC, Warinner C "Successful enrichment and recovery of whole mitochondrial genomes from ancient human dental calculus" American Journal of Physical Anthropology , v.160 , 2016 , p.220 10.1002/ajpa.22960
Schnorr S, Sankaranarayanan K, Lewis CM, and Warinner C "Insights into human evolution from ancient and contemporary microbiome studies" Current Opinion in Genetics and Development , 2016
Schnorr S, Sankaranarayanan K, Lewis CM, Warinner C "Insights into human evolution from ancient and contemporary microbiome studies" Current Opinion in Genetics and Development , v.41 , 2016 10.1016/j.gde.2016.07.003
Schnorr, Stephanie L and Sankaranarayanan, Krithivasan and Lewis, Cecil M and Warinner, Christina "Insights into human evolution from ancient and contemporary microbiome studies" Current Opinion in Genetics & Development , v.41 , 2016 10.1016/j.gde.2016.07.003 Citation Details
Velsko IM, Frantz LAF, Herbig A, Larson G, Warinner C "Selection of appropriate metagenome taxonomic classifiers for ancient microbiome research" mSystems , v.3 , 2018 , p.e00080-18 10.1128/mSystems.00080-18
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 "The dental calculus metabolome in modern and historic samples." Metabolomics , 2017 10.1007/s11306-017-1270-3
(Showing: 1 - 10 of 20)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

This funding supported the investigation of the evolution and ecology of the human oral microbiome. Recently, our research team demonstrated that calcified dental plaque, also known as  tooth tartar or dental calculus, is a robust and long-term reservoir of DNA from the oral microbiome. Being mineralized, dental calculus is resistant to decay, but until now it was not known how long DNA survived in dental calculus or what insights might be gained about the history and origins of oral microbiome-associated diseases, such as periodontal disease and caries, by studying this substrate in archaeological and historical skeletal collections. Focusing on an extraordinary set of more than 300 dental calculus samples obtained from New World monkeys (howler monkeys), great apes (gorillas, chimpanzees), Neanderthals, and humans (Paleolithic through present-day), we document the evolution of the oral microbiome in the hominoid lineage. We find that by applying advanced ancient DNA technologies, authentic DNA from the oral microbiome can be successfully recovered from dental calculus samples more than 70,000 years old. Through this research we describe the core hominoid oral microbiome, define the bacterial taxa and ecological patterns that characterize specific primate species, and establish the antiquity of periodontal pathogens. We show that oral bacteria generally exhibit patterns of co-speciation with their hosts, and that the genetic diversity of oral bacteria in Neanderthals is distinct from that of the great apes and typically falls within the range of variation of anatomically modern humans. We additionally find that contrary to previous studies, health-associated bacterial taxa, such as Streptococcus and Neisseria, are more abundant in calculus today than in the past, which may be the result of modern oral hygiene regimens. We also find that Tannerella forsythia, a species associated today with periodontal disease, was both prevalent and abundant in past human populations - irrespective of disease - and that it is today found at relatively high levels in living chimpanzee populations. Finally, our findings additionally call into question whether bacterial species conventionally regarded in clinical contexts as pathogenic, such as Porphyromonas gingivalisTreponema denticolaTannerella forsythiaMethanobrevibacter oralis, and Desulfobulbus spp., are in fact causal of pathology or simply markers of biofilm maturity. Such findings have broad-scale implications for the diagnosis of periodontal diseases and their treatment. In addition to these main findings, we have also published the first major study of small molecule metabolite preservation in dental calculus, and we have substantially contributed to the understanding of protein preservation in dental calculus. To date, this project has resulted in 14 conference presentations and 12 peer-reviewed publications, of which 9 are open access publications, and all genetic and proteomic data associated with project publications have been made available through public repositories. This project has contributed to the STEM training of three postdocs, six PhD students, and two Master's students. Finally, this project has resulted in 15 public lectures, contributed to K-12 educational material made available on the PI's research website, and contributed to interactive exhibits on genetics and microscopy at K-12 public science education events. 

 

 


Last Modified: 10/05/2018
Modified by: Christina G Warinner

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