doi: 10.1038/s41467-019-12154-0.
Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes
Maria A Spyrou 1 2, Marcel Keller 3 4, Rezeda I Tukhbatova 3 5, Christiana L Scheib 6, Elizabeth A Nelson 3 7, Aida Andrades Valtueña 3, Gunnar U Neumann 3, Don Walker 8, Amelie Alterauge 9, Niamh Carty 8, Craig Cessford 10, Hermann Fetz 11, Michaël Gourvennec 12, Robert Hartle 8, Michael Henderson 8, Kristin von Heyking 4, Sarah A Inskip 13, Sacha Kacki 14 15, Felix M Key 16, Elizabeth L Knox 8, Christian Later 17, Prishita Maheshwari-Aplin 10, Joris Peters 4 18, John E Robb 10, Jürgen Schreiber 19, Toomas Kivisild 6 20, Dominique Castex 14, Sandra Lösch 9, Michaela Harbeck 4, Alexander Herbig 3, Kirsten I Bos 21, Johannes Krause 22 23
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- PMID:31578321
- PMCID: PMC6775055
- DOI: 10.1038/s41467-019-12154-0
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Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes
Maria A Spyrou et al. Nat Commun..
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Abstract
The second plague pandemic, caused by Yersinia pestis, devastated Europe and the nearby regions between the 14th and 18th 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.
Conflict of interest statement
The authors declare no competing interests.
Figures
Archaeological site locations and chronologies.a Map showing the geographic locations of archaeological sites from which second pandemic (14th- to 18th-century AD)Y. pestis genomes have been reconstructed (≥1-fold). The number (n) of genomes obtained from each site is shown in brackets. Locations of previously published genomes appear in triangles, whereas genomes that are newly described in this study appear in circles (labels in bold). Base map purchased from [vectormaps.de].b Specimen chronologies combining archaeological and radiocarbon dates of previously published and new second plague pandemic isolates (see Supplementary Note 1 and Supplementary Table 3)
Phylogenetic positioning of second pandemic strains. A maximum likelihood phylogeny was generated allowing for up to 3% missing data (97% partial deletion) and considering a total of 6,058 single nucleotide polymorphisms (SNPs). The image shows a graphical representation of Branches 1–4 (see Supplementary Fig. 12 for a complete phylogeny), to emphasise the phylogenetic positioning of the new and previously published second pandemic strains (labels of new 14th- to 17th-century strains appear in bold). Dashed branches denote uncertainty in the private SNP calls of the respective genomes. Sub-clades of published genomes are collapsed to enhance tree visibility. Numbers (n) in brackets indicate the number of strains represented in each collapsed branch. Node support was estimated using 1,000 bootstrap iterations. Nodes that have bootstrap values of ≥95 are indicated by asterisks (*). Scale denotes substitutions per site. Geographic abbreviations of modern strain isolation locations are as follows: China (CHN), United States of America (USA), Madagascar (MDG), India (IND), Myanmar (MNM), Congo (COG), Uganda (UGA), Mongolia (MNG), Nepal (NPL), Iran (IRN), Kazakhstan (KAZ), Kyrgyzstan (KGZ), Tajikistan (TJK), Armenia (ARM), Georgia (GEO), Azerbaijan (AZE), Uzbekistan (UZB), Turkmenistan (TKM), Russia (RUS) and unspecified regions of the Former Soviet Union (FSU)
Substitution rate variation across theY. pestis Branch 1. The figure presents a maximum clade credibility (MCC) phylogenetic tree generated using BEAST v1.8 (rooted with 2.MED KIM10—outgroup not shown). The tree was viewed in FigTree v1.4 (http://tree.bio.ed.ac.uk/software/figtree/ ), and modified so that branch colours represent mean substitution rates (substitutions per site per year). The tree depicts the substitution rate variation across Branch 1 of theY. pestis phylogeny, which ranges from 2.09E–7 (highest-red) to 4.95E–9 (lowest-blue) substitutions per site per year (see rate key). The isolates used for this analysis overlap with the ones used for the SNP and maximum likelihood phylogenetic analysis (see Supplementary Fig. 12), with the exception of the TRP002 and OSL1 genomes since their private SNP calls are likely affected by environmental contamination and other representative genomes exist in our dataset from the BD time period (1346–1353 AD). Labels of genomes associated with the second and third plague pandemics appear in bold. The mean substitution rate across the tree (including 2.MED KIM10) was calculated to 2.85E–8 substitutions per site per year. Lengths of branches are scaled to represent sample ages, and the depicted Branch 1 sequences are estimated to represent 731 years (95% HPD: 672–823) ofY. pestis evolution. The time scale is shown in years before the present (BP), where present denotes the most recently isolated modernY. pestis strain (year 2005)
Assessment of chromosomal and gene-specific coverage inY. pestis.a A comparison of genetic profiles was performed across newly reconstructed and previously published second pandemic genomes (in red, orange, green and blue). Here, we show an assessment of the presence or absence of 80 previously defined potential virulence and evolutionary determinants across theY. pestis chromosome. Published genomes from the Bronze Age period, (RISE509 and RT5), from the first pandemic (6th-century Altenerding 2148), from modern-day isolates (0.PE2, 0.PE4 and 1.ORI), as well asY. pseudotuberculosis IP32953, are also shown for comparative purposes. The colour scale ranges from 0 (not covered—yellow) to 1 (entirely covered—blue) according to the relative proportion of gene/locus covered. The heatmap was plotted in R version 3.4.1 using the ggplot2 package. Boxes marked with “X” indicate genomic loci that were not part of theY. pestis probe design when the respective isolates were captured,. Refer to Supplementary Fig. 20 for presence/absence of virulence-associated genes across the pMT1, pPCP1 and pCD1 plasmids.b Chromosomal coverage plots made with the Circos software. The plots were constructed to a maximum coverage of 20-fold, and the average coverage was calculated over 3,000-bp windows. Genomes are shown in chronological order from oldest (innermost circle) to youngest (outermost circle) as follows: LAI009, London BD 8124/8291/11972 (BD representative), Ber45, Bolgar 2370, MAN008, STA001, NMS002, ELW098/549_O, LBG002, STN014, BRA002, BED030, OBS137 and the reference genome CO92. The outermost ring represents fluctuations in GC content (%) across CO92, where dark and light grey bars show deviations from the genomic mean (47.6%) by at least one standard deviation
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References
- Benedictow, O. J. The Black Death, 1346-1353: The Complete History (Boydell and Brewer, Woodbridge, UK, and Rochester, N.Y., 2004).
- 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).