Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the First Pandemic (541–750)

The first historically documented pandemic caused by Yersinia pestis began as the Justinianic Plague in 541 within the Roman Empire and continued as the so-called First Pandemic until 750. Although paleogenomic studies have previously identified the causative agent as Y. pestis, little is known abou...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 25; pp. 12363 - 12372
Main Authors: Keller, Marcel, Spyrou, Maria A., Scheib, Christiana L., Neumann, Gunnar U., Kröpelin, Andreas, Haas-Gebhard, Brigitte, Päffgen, Bernd, Haberstroh, Jochen, Lacombai, Albert Ribera i, Raynaud, Claude, Cessford, Craig, Durand, Raphaël, Stadler, Peter, Nägele, Kathrin, Bates, Jessica S., Trautmann, Bernd, Inskip, Sarah A., Peters, Joris, Robb, John E., Kivisild, Toomas, Castex, Dominique, McCormick, Michael, Bos, Kirsten I., Harbeck, Michaela, Herbig, Alexander, Kraus, Johannes
Format: Journal Article
Language:English
Published: United States National Academy of Sciences 18-06-2019
Series:PNAS Plus
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Summary:The first historically documented pandemic caused by Yersinia pestis began as the Justinianic Plague in 541 within the Roman Empire and continued as the so-called First Pandemic until 750. Although paleogenomic studies have previously identified the causative agent as Y. pestis, little is known about the bacterium’s spread, diversity, and genetic history over the course of the pandemic. To elucidate the microevolution of the bacterium during this time period, we screened human remains from 21 sites in Austria, Britain, Germany, France, and Spain for Y. pestis DNA and reconstructed eight genomes. We present a methodological approach assessing single-nucleotide polymorphisms (SNPs) in ancient bacterial genomes, facilitating qualitative analyses of low coverage genomes from a metagenomic background. Phylogenetic analysis on the eight reconstructed genomes reveals the existence of previously undocumented Y. pestis diversity during the sixth to eighth centuries, and provides evidence for the presence of multiple distinct Y. pestis strains in Europe. We offer genetic evidence for the presence of the Justinianic Plague in the British Isles, previously only hypothesized from ambiguous documentary accounts, as well as the parallel occurrence of multiple derived strains in central and southern France, Spain, and southern Germany. Four of the reported strains form a polytomy similar to others seen across the Y. pestis phylogeny, associated with the Second and Third Pandemics. We identified a deletion of a 45-kb genomic region in the most recent First Pandemic strains affecting two virulence factors, intriguingly overlapping with a deletion found in 17th- to 18th-century genomes of the Second Pandemic.
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1M.K. and M.A.S. contributed equally to this work.
Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved May 9, 2019 (received for review November 30, 2018)
3Present address: Institute of Genomics, University of Tartu, 51010 Tartu, Estonia.
Author contributions: M.M., K.I.B., M.H., A.H., and J.K. designed the study; M.K., M.A.S., C.L.S., G.U.N., K.N., and J.S.B. performed laboratory work; A.K. developed the new analytical tool; M.K., M.A.S., and G.U.N. performed data analyses; B.T. and S.A.I. performed anthropological examination; C.L.S. and T.K. provided genomic data; B.H.-G., B.P., J.H., A.R.i.L., C.R., P.S., J.P., J.E.R., D.C., and M.H. identified and provided access to archaeological material; B.H.-G., B.P., J.H., A.R.i.L., C.R., C.C., R.D., P.S., and M.M. provided archaeological and historical information; and M.K., M.A.S., M.M., and A.H. wrote the paper with contributions from all authors.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1820447116