The DOI matches its Crossref record; 8 of the 8 references it cites were found in a registry or an index.
Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes
Open accessAbstract
The second plague pandemic, caused by Yersinia pestis , devastated Europe and the nearby regions between the 14 th and 18 th centuries AD. Here we analyse human remains from ten European archaeological sites spanning this period and reconstruct 34 ancient Y. pestis genomes. Our data support an initial entry of the bacterium through eastern Europe, the absence of genetic diversity during the Black Death, and low within-outbreak diversity thereafter. Analysis of post-Black Death genomes shows the diversification of a Y. pestis lineage into multiple genetically distinct clades that may have given rise to more than one disease reservoir in, or close to, Europe. In addition, we show the loss of a genomic region that includes virulence-related genes in strains associated with late stages of the pandemic. The deletion was also identified in genomes connected with the first plague pandemic (541–750 AD), suggesting a comparable evolutionary trajectory of Y. pestis during both events.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Analyses of the victims of both the Plague of Justinian and the Black Death have shown that Y. pestis was indeed the cause of both pandemics, and further genomic analysis has provided insight into the course of these pandemics over time, including parallel changes in the pathogen itself.
“For example, analyses of the victims of both the Plague of Justinian and the Black Death have shown that Y. pestis was indeed the cause of both pandemics 65,303 , and further genomic analysis has provided insight into the course of these pandemics over time, including parallel changes in the pathogen itself [304][305][306] .”
From Ancient DNA analysis (2021) · cites this paper as [303]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447
mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters
Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F., & Orlando, L. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt193 · Cited by 1,669
Dabney, J., Knapp, M., Glocke, I., Gansauge, M.-T., Weihmann, A., Nickel, B., Valdiosera, C., García, N., Pääbo, S., Arsuaga, J.-L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314445110 · Cited by 1,443
Yersinia pestis , the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis
Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., & Carniel, E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.24.14043 · Cited by 1,126
Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform
Kircher, M., Sawyer, S., & Meyer, M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr771 · Cited by 1,106
Partial uracil–DNA–glycosylase treatment for screening of ancient DNA
Rohland, N., Harney, E., Mallick, S., Nordenfelt, S., & Reich, D. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0624 · Cited by 572
The genome of a Late Pleistocene human from a Clovis burial site in western Montana
Rasmussen, M., Anzick, S. L., Waters, M. R., Skoglund, P., DeGiorgio, M., Stafford, T. W., Rasmussen, S., Moltke, I., Albrechtsen, A., Doyle, S. M., et al. (2014) · Nature · doi:10.1038/nature13025 · Cited by 562
Living standards and plague in London, 1560–1665
Cummins, N., Kelly, M., & Ó Gráda, C. (2016) · The Economic History Review · doi:10.1111/ehr.12098 · Cited by 139
Flagged first, then by citations
Research works printed but not linked: 77
- Biraben, J.-N. Les Hommes et la peste en France et dans les pays européens et méditerranéens. t. 2, les hommes face à la peste (Mouton, Paris, 1976). · DOI
- Parkhill, J. et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523–527 (2001). · DOI
- Gage, K. L. & Kosoy, M. Y. Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol. 50, 505–528 (2005). · DOI
- Prentice, M. B. & Rahalison, L. Plague. Lancet 369, 1196–1207 (2007). · DOI
- Alexander, J. T. Bubonic Plague in Early Modern Russia: Public Health and Urban Disaster (Johns Hopkins University Press, Baltimore, Maryland, USA, 1980).
- Namouchi, A. et al. Integrative approach using Yersinia pestis genomes to revisit the historical landscape of plague during the Medieval Period. Proc. Natl Acad. Sci. USA 115, E11790–E11797 (2018). · DOI
- Spyrou, M. A. et al. Historical Y. pestis genomes reveal the European Black Death as the source of ancient and modern plague pandemics. Cell Host Microbe 19, 874–881 (2016). · DOI
- Bos, K. I. et al. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506–510 (2011). · DOI · Paper page
- Büntgen, U., Ginzler, C., Esper, J., Tegel, W. & McMichael, A. J. Digitizing historical plague. Clin. Infect. Dis. 55, 1586–1588 (2012). · DOI
- Schmid, B. V. et al. Climate-driven introduction of the Black Death and successive plague reintroductions into Europe. Proc. Natl Acad. Sci. USA 112, 3020–3025 (2015). · DOI
- Seifert, L. et al. Genotyping Yersinia pestis in historical plague: evidence for long-term persistence of Y. pestis in Europe from the 14th to the 17th Century. PLoS ONE 11, e0145194 (2016). · DOI
- Bos, K. I. et al. Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. eLife 5, e12994 (2016). · DOI
- Morelli, G. et al. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 42, 1140–1143 (2010). · DOI
- Schuenemann, V. J. et al. Targeted enrichment of ancient pathogens yielding the pPCP1 plasmid of Yersinia pestis from victims of the Black Death. Proc. Natl Acad. Sci. USA 108, E746–E752 (2011). · DOI
- Vågene, A. J. et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nat. Ecol. Evol. 2, 520–528 (2018). · DOI
- Huebler, R. et al. HOPS: automated detection and authentication of pathogen DNA in archaeological remains. Preprint at https://www.biorxiv.org/content/10.1101/534198v2 (2019). · DOI · Paper page
- Briggs, A. W. et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 38, e87 (2010). · DOI · Paper page
- Meyer, M. & Kircher, M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010, pdb.prot5448 (2010). · DOI
- Andrades Valtueña, A. et al. The Stone Age plague and its persistence in Eurasia. Curr. Biol. 27, 3683–3691 (2017). e3688. · DOI
- Cui, Y. et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl Acad. Sci. USA 110, 577–582 (2013). · DOI
- Kislichkina, A. A. et al. Nineteen whole-genome assemblies of Yersinia pestis subsp. microtus, including representatives of Biovars caucasica, talassica, hissarica, altaica, xilingolensis, and ulegeica. Genome Announc. 3, e01342–01315 (2015). · DOI
- Zhgenti, E. et al. Genome assemblies for 11 Yersinia pestis strains isolated in the Caucasus region. Genome Announc. 3, e01030–01015 (2015). · DOI
- Kutyrev, V. V. et al. Phylogeny and classification of Yersinia pestis through the lens of strains from the plague foci of Commonwealth of Independent States. Front. Microbiol. 9, 1106 (2018). · DOI
- Eroshenko, G. A. et al. Yersinia pestis strains of ancient phylogenetic branch 0. ANT are widely spread in the high-mountain plague foci of Kyrgyzstan. PLoS ONE 12, e0187230 (2017). · DOI
- Keller, M. et al. Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the First Pandemic (541-750 CE). Proc. Natl Acad. Sci. USA 116, 12363–12372 (2019). · DOI · Paper page
- Feldman, M. et al. A high-coverage Yersinia pestis genome from a sixth-century Justinianic plague victim. Mol. Biol. Evol. 33, 2911–2923 (2016). · DOI
- de Barros Damgaard, P. et al. 137 ancient human genomes from across the Eurasian steppes. Nature 557, 369 (2018). · DOI
- Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015). · DOI
- Spyrou, M. A. et al. Analysis of 3800-year-old Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat. Commun. 9, 2234 (2018). · DOI
- Bos, K. I. et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014). · DOI · Paper page
- Darling, A. E., Miklós, I. & Ragan, M. A. Dynamics of genome rearrangement in bacterial populations. PLoS Genet. 4, e1000128 (2008). · DOI
- Green, M. H. Putting Africa on the Black Death map: Narratives from genetics and history. Afriques (2018). Available at: http://journals.openedition.org/afriques/2125 (Accessed: 3rd September 2019). · DOI
- Zhou, D. & Yang, R. Molecular Darwinian evolution of virulence in Yersinia pestis. Infect. Immun. 77, 2242–2250 (2009). · DOI
- Zhou, D. et al. Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J. Bacteriol. 186, 5147–5152 (2004). · DOI
- Simonet, M., Riot, B., Fortineau, N. & Berche, P. Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect. Immun. 64, 375–379 (1996). · DOI
- Groisman, E. A. et al. Bacterial Mg2+ homeostasis, transport, and virulence. Annu. Rev. Genet. 47, 625–646 (2013). · DOI
- Ford, D. C., Joshua, G. W., Wren, B. W. & Oyston, P. C. The importance of the magnesium transporter MgtB for virulence of Yersinia pseudotuberculosis and Yersinia pestis. Microbiology 160, 2710–2717 (2014). · DOI
- Fetherston, J. D. & Perry, R. D. The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol. Microbiol. 13, 697–708 (1994). · DOI
- Signoli, M., Bello, S. & Dutour, O. [Epidemic recrudescence of the Great Plague in Marseille (May-July 1722): excavation of a mass grave]. Med. Trop. (Mars) 58, 7–13 (1998).
- Wagner, D. M. et al. Yersinia pestis and the Plague of Justinian 541–543 AD: a genomic analysis. Lancet Infect. Dis. 14, 319–326 (2014). · DOI
- Benedictow, O. J. The Black Death and Later Plague Epidemics in the Scandinavian Countries: Perspectives and Controversies (Walter de Gruyter GmbH & Co KG, Warsaw/Berlin, 2016). · DOI
- Spyrou, M. A., Bos, K. I., Herbig, A. & Krause, J. Ancient pathogen genomics as an emerging tool for infectious disease research. Nat. Rev. Genet. 20, 323–340 (2019). · DOI · Paper page
- Hymes, R. Epilogue: a hypothesis on the East Asian beginnings of the Yersinia pestis polytomy. in Pandemic Disease in the Medieval World: Rethinking the Black Death Vol. 1 (ed. Green, M. H.) 285–308 (Arc Medieval Press, Kalamazoo and Bradford, 2014). · DOI
- Haensch, S. et al. Distinct clones of Yersinia pestis caused the black death. PLoS Pathog. 6, e1001134 (2010). · DOI
- Chain, P. S. et al. Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J. Bacteriol. 188, 4453–4463 (2006). · DOI
- Carmichael, A. G. Plague persistence in Western Europe: a hypothesis. in Pandemic Disease in the Medieval World: Rethinking the Black Death Vol. 1 (ed. Green, M. H.) 157–191 (Arc Medieval Press, Kalamazoo and Bradford, 2014). · DOI
- Signoli, M., Séguy, I., Biraben, J.-N., Dutour, O. & Belle, P. Paleodemography and historical demography in the context of an epidemic. Population 57, 829–854 (2002).
- Vogler, A. J. et al. Temporal phylogeography of Yersinia pestis in Madagascar: insights into the long-term maintenance of plague. PLOS Negl. Trop. Dis. 11, e0005887 (2017). · DOI
- Grabenstein, J. P., Fukuto, H. S., Palmer, L. E. & Bliska, J. B. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74, 3727–3741 (2006). · DOI
- Blanc‐Potard, A. B. & Groisman, E. A. The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J. 16, 5376–5385 (1997). · DOI
- Snavely, M., Miller, C. & Maguire, M. The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J. Biol. Chem. 266, 815–823 (1991). · DOI
- Belon, C. et al. A macrophage subversion factor is shared by intracellular and extracellular pathogens. PLoS Pathog. 11, e1004969 (2015). · DOI
- Snavely, M., Florer, J., Miller, C. & Maguire, M. Magnesium transport in Salmonella typhimurium: 28Mg2+ transport by the CorA, MgtA, and MgtB systems. J. Bacteriol. 171, 4761–4766 (1989). · DOI
- Chain, P. S. et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl Acad. Sci. USA 101, 13826–13831 (2004). · DOI
- Perry, R. D. & Fetherston, J. D. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10, 35–66 (1997). · DOI
- Dean, K. R. et al. Human ectoparasites and the spread of plague in Europe during the Second Pandemic. Proc. Natl Acad. Sci. USA 115, 1304–1309 (2018). · DOI
- Keeling, M. K. & Gilligan, C. A. Metapopulation dynamics of bubonic plague. Nature 407, 903–906 (2000). · DOI
- Xu, L. et al. The trophic responses of two different rodent–vector–plague systems to climate change. Proc. Biol. Sci. 282, 20141846 (2015). · DOI
- Xu, L. et al. Wet climate and transportation routes accelerate spread of human plague. Proc. Biol. Sci. 281, 20133159 (2014). · DOI
- Whittles, L. K. & Didelot, X. Epidemiological analysis of the Eyam plague outbreak of 1665–1666. Proc. Biol. Sci. 283, 20160618 (2016). · DOI
- Roosen, J. & Curtis, D. R. Dangers of noncritical use of historical plague data. Emerg. Infect. Dis. 24, 103 (2018). · DOI
- Peltzer, A. et al. EAGER: efficient ancient genome reconstruction. Genome Biol. 17, 60 (2016). · DOI · Paper page
- Schubert, M., Lindgreen, S. & Orlando, L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016). · DOI
- Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010). · DOI · Paper page
- DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011). · DOI
- Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly ( Austin ) 6, 80–92 (2012). · DOI · Paper page
- Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016). · DOI
- Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). · DOI · Paper page
- Tavaré, S. Some probabilistic and statistical problems in the analysis of DNA sequences. in Lectures on Mathematics in the Life Sciences Vol. 17 (ed. Miura, R. M.) 57–86 (American Mathematical Society, Providence, Rhode Island, 1986).
- Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013). · arXiv
- Auerbach, R. K. et al. Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America. PLoS ONE 2, e770 (2007). · DOI
- Eppinger, M. et al. Draft genome sequences of Yersinia pestis isolates from natural foci of endemic plague in China. J. Bacteriol. 191, 7628–7629 (2009). · DOI
- Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007). · DOI
- Kingman, J. F. C. The coalescent. Stoch. Process. Appl. 13, 235–248 (1982). · DOI
- Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192 (2005). · DOI
- Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010). · DOI · Paper page
- Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009). · DOI
Cited by
Sorted by citations
Orlando, L., Allaby, R., Skoglund, P., Der Sarkissian, C., Stockhammer, P. W., Ávila-Arcos, M. C., Fu, Q., Krause, J., Willerslev, E., Stone, A. C., et al. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-020-00011-0 · Cited by 411
Self-citation
Metadata
- Authors
- Spyrou, M. A., Keller, M., Tukhbatova, R. I., Scheib, C. L., Nelson, E. A., Andrades Valtueña, A., Neumann, G. U., Walker, D., Alterauge, A., Carty, N., Cessford, C., Fetz, H., Gourvennec, M., Hartle, R., Henderson, M., von Heyking, K., Inskip, S. A., Kacki, S., Key, F. M., Knox, E. L., Later, C., Maheshwari-Aplin, P., Peters, J., Robb, J. E., Schreiber, J., Kivisild, T., Castex, D., Lösch, S., Harbeck, M., Herbig, A., Bos, K. I., & Krause, J.
- Affiliations
- Max Planck Institute of Geoanthropology (DE)
- University of Tartu (EE)
- Museum of London Archaeology (GB)
- University of Bern (CH)
- University of Cambridge (GB)
- Staatsarchiv Nidwalden (CH)
- Bavarian Natural History Collections (DE)
- Centre National de la Recherche Scientifique (FR)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Spyrou, Maria A.
- Bos, Kirsten I.
- Krause, Johannes
- ORCID
- Spyrou, Maria A.
- Keller, Marcel
- Scheib, Christiana L.
- Nelson, Elizabeth A.
- Andrades Valtueña, Aida
- Neumann, Gunnar U.
- Walker, Don
- Alterauge, Amelie
- Cessford, Craig
- Gourvennec, Michaël
- Inskip, Sarah A.
- Kacki, Sacha
- Key, Felix M.
- Peters, Joris
- Robb, John E.
- Kivisild, Toomas
- Castex, Dominique
- Lösch, Sandra
- Harbeck, Michaela
- Herbig, Alexander
- Bos, Kirsten I.
- Krause, Johannes
- Venue
- Nature Communications
- Published
- 2019-10-02
- Volume
- 10
- Issue
- 1
- Pages
- 4470-4470
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC6775055
- OpenAlex
- W2978619983
- Cited by
- 182
- References
- 8
- Citations by year
- 2026: 17 · 2025: 17 · 2024: 31 · 2023: 26 · 2022: 31 · 2021: 30 · 2020: 24 · 2019: 6
- FWCI
- 17.68
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Durham Research Online (Durham University) (acceptedVersion, other-oa)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Durham Research Online (Durham University) (submittedVersion, cc-by)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- HAL (submittedVersion)
- HAL (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- University of Bern
- Wellcome Trust (200368/Z/15/Z)
- European Commission (2014‐2020, 2020 ‘, 2014-2020.4.01.16-0030)
- Eesti Teadusagentuur (PRG243, 2014-2020)
- Queen's University
- Max-Planck-Gesellschaft
- European Regional Development Fund (2014-2020’, 2014-2020.4.01.16-0030)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Yersinia bacterium, plague, ectoparasites research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Keywords
- Yersinia pestis, Black Death, second plague pandemic, phylogeography, ancient genomes, human remains, genetic diversity, virulence gene deletion, disease reservoirs, bacterial evolution
- MeSH terms
- Archaeology, DNA, Bacterial, Europe, Eastern, Fossils, Humans, Phylogeny, Plague, Time Factors, Virulence, Yersinia pestis, Genome, Bacterial, Polymorphism, Single Nucleotide, Pandemics, Phylogeography, High-Throughput Nucleotide Sequencing
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review