Improving the Extraction of Ancient Genomes from the Dental Pulp

Overview

Journal iScience

Publisher Cell Press

Date 2023 May 30

PMID 37250315

Authors

Pierre Clavel

Lexane Louis

Clio Der Sarkissian

Catherine Theves

Claudia Gillet

Lorelei Chauvey

Gaetan Tressieres

Stephanie Schiavinato

Laure Calviere-Tonasso

Norbert Telmon

Benoit Clavel

Richard Jonvel

Stefan Tzortzis

Laetitia Bouniol

Jean-Marc Femolant

Jennifer Klunk

Hendrik Poinar

Michel Signoli

Caroline Costedoat

Maria A Spyrou

Andaine Seguin-Orlando

Ludovic Orlando

Affiliations

Soon will be listed here.

Abstract

Ancient DNA preserved in the dental pulp offers the opportunity to characterize the genome of some of the deadliest pathogens in human history. However, while DNA capture technologies help, focus sequencing efforts, and therefore, reduce experimental costs, the recovery of ancient pathogen DNA remains challenging. Here, we tracked the kinetics of ancient DNA release in solution during a pre-digestion of the dental pulp. We found that most of the ancient DNA is released within 60 min at 37°C in our experimental conditions. We recommend a simple pre-digestion as an economical procedure to obtain extracts enriched in ancient pathogen DNA, as longer digestion times release other types of templates, including host DNA. Combining this procedure with DNA capture, we characterized the genome sequences of 12 ancient bacteria from France dating to the second pandemic outbreaks of the 17 and 18 centuries Common Era.

Citing Articles

The Natural and Clinical History of Plague: From the Ancient Pandemics to Modern Insights.

Bennasar-Figueras A Microorganisms. 2024; 12(1).

PMID: 38257973 PMC: 10818976. DOI: 10.3390/microorganisms12010146.

References

Tzortzis S, Signoli M . Characterization of the Funeral Groups Associated with Plague Epidemics. Microbiol Spectr. 2016; 4(4). DOI: 10.1128/microbiolspec.PoH-0011-2015. View

Groisman E, Hollands K, Kriner M, Lee E, Park S, Pontes M . Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet. 2013; 47:625-46. PMC: 4059682. DOI: 10.1146/annurev-genet-051313-051025. View

Wang H, Avican K, Fahlgren A, Erttmann S, Nuss A, Dersch P . Increased plasmid copy number is essential for Yersinia T3SS function and virulence. Science. 2016; 353(6298):492-5. DOI: 10.1126/science.aaf7501. View

Margaryan A, Hansen H, Rasmussen S, Sikora M, Moiseyev V, Khoklov A . Ancient pathogen DNA in human teeth and petrous bones. Ecol Evol. 2018; 8(6):3534-3542. PMC: 5869295. DOI: 10.1002/ece3.3924. View

Keller M, Spyrou M, Scheib C, Neumann G, Kropelin A, Haas-Gebhard B . Ancient genomes from across Western Europe reveal early diversification during the First Pandemic (541-750). Proc Natl Acad Sci U S A. 2019; 116(25):12363-12372. PMC: 6589673. DOI: 10.1073/pnas.1820447116. View

Yu H, Spyrou M, Karapetian M, Shnaider S, Radzeviciute R, Nagele K . Paleolithic to Bronze Age Siberians Reveal Connections with First Americans and across Eurasia. Cell. 2020; 181(6):1232-1245.e20. DOI: 10.1016/j.cell.2020.04.037. View

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

Fages A, Hanghoj K, Khan N, Gaunitz C, Seguin-Orlando A, Leonardi M . Tracking Five Millennia of Horse Management with Extensive Ancient Genome Time Series. Cell. 2019; 177(6):1419-1435.e31. PMC: 6547883. DOI: 10.1016/j.cell.2019.03.049. View

Bos K, Kuhnert D, Herbig A, Esquivel-Gomez L, Andrades Valtuena A, Barquera R . Paleomicrobiology: Diagnosis and Evolution of Ancient Pathogens. Annu Rev Microbiol. 2019; 73:639-666. DOI: 10.1146/annurev-micro-090817-062436. View

10.

Ziesemer K, Ramos-Madrigal J, Mann A, Brandt B, Sankaranarayanan K, Ozga A . The efficacy of whole human genome capture on ancient dental calculus and dentin. Am J Phys Anthropol. 2018; 168(3):496-509. PMC: 6519167. DOI: 10.1002/ajpa.23763. View

11.

Andrades Valtuena A, Mittnik A, Key F, Haak W, Allmae R, Belinskij A . The Stone Age Plague and Its Persistence in Eurasia. Curr Biol. 2017; 27(23):3683-3691.e8. DOI: 10.1016/j.cub.2017.10.025. View

12.

Schubert M, Lindgreen S, Orlando L . AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes. 2016; 9:88. PMC: 4751634. DOI: 10.1186/s13104-016-1900-2. View

13.

Yu T, Keto-Timonen R, Jiang X, Virtanen J, Korkeala H . Insights into the Phylogeny and Evolution of Cold Shock Proteins: From Enteropathogenic and to Eubacteria. Int J Mol Sci. 2019; 20(16). PMC: 6719143. DOI: 10.3390/ijms20164059. View

14.

van Dorp L, Gelabert P, Rieux A, de Manuel M, de-Dios T, Gopalakrishnan S . Plasmodium vivax Malaria Viewed through the Lens of an Eradicated European Strain. Mol Biol Evol. 2019; 37(3):773-785. PMC: 7038659. DOI: 10.1093/molbev/msz264. View

15.

Ferrari G, Neukamm J, Baalsrud H, Breidenstein A, Ravinet M, Phillips C . Variola virus genome sequenced from an eighteenth-century museum specimen supports the recent origin of smallpox. Philos Trans R Soc Lond B Biol Sci. 2020; 375(1812):20190572. PMC: 7702794. DOI: 10.1098/rstb.2019.0572. View

16.

Der Sarkissian C, Ermini L, Jonsson H, Alekseev A, Crubezy E, Shapiro B . Shotgun microbial profiling of fossil remains. Mol Ecol. 2014; 23(7):1780-98. DOI: 10.1111/mec.12690. View

17.

Gamba C, Hanghoj K, Gaunitz C, Alfarhan A, Alquraishi S, Al-Rasheid K . Comparing the performance of three ancient DNA extraction methods for high-throughput sequencing. Mol Ecol Resour. 2015; 16(2):459-69. DOI: 10.1111/1755-0998.12470. View

18.

Rasmussen M, Li Y, Lindgreen S, Pedersen J, Albrechtsen A, Moltke I . Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature. 2010; 463(7282):757-62. PMC: 3951495. DOI: 10.1038/nature08835. View

19.

Susko E, Roger A . Long Branch Attraction Biases in Phylogenetics. Syst Biol. 2021; 70(4):838-843. DOI: 10.1093/sysbio/syab001. View

20.

Cruz-Davalos D, Llamas B, Gaunitz C, Fages A, Gamba C, Soubrier J . Experimental conditions improving in-solution target enrichment for ancient DNA. Mol Ecol Resour. 2016; 17(3):508-522. DOI: 10.1111/1755-0998.12595. View