Analysis of the Three Yersinia pestis CRISPR Loci Provides New Tools for Phylogenetic Studies and Possibly for the Investigation of Ancient DNA

Abstract Plague has an enigmatic history as a zoonotic pathogen. This potentially devastating infectious disease will unexpectedly appear in human populations and disappear just as suddenly. As a result, a long-standing line of inquiry has been to estimate when and where plague appeared in the past. However, there have been significant disparities between phylogenetic studies of the causative bacterium, Yersinia pestis, regarding the timing and geographic origins of its reemergence. Here, we curate and contextualize an updated phylogeny of Y. pestis using 601 genome sequences sampled globally. We perform a detailed Bayesian evaluation of temporal signal in subsets of these data and demonstrate that a Y. pestis-wide molecular clock model is unstable. To resolve this, we devised a new approach in which each Y. pestis population was assessed independently. This enabled us to recover significant temporal signal in five populations, including the ancient pandemic lineages which we now estimate may have emerged decades, or even centuries, before a pandemic was historically documented from European sources. Despite this, we only obtain robust divergence dates from populations sampled over a period of at least 90 years, indicating that genetic evidence alone is insufficient for accurately reconstructing the timing and spread of short-term plague epidemics. Finally, we identify key historical data sets that can be used in future research, which will complement the strengths and mitigate the weaknesses of genomic data.

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Beyond Plague Pits: Using Genetics to Identify Responses to Plague in Medieval Cambridgeshire

European Journal of Archaeology ◽

10.1017/eaa.2021.19 ◽

2021 ◽

pp. 1-23

Author(s):

Craig Cessford ◽

Christiana L. Scheib ◽

Meriam Guellil ◽

Marcel Keller ◽

Craig Alexander ◽

...

Keyword(s):

Yersinia Pestis ◽

Ancient Dna ◽

Major Advance ◽

Mass Graves ◽

Detailed Consideration ◽

The Creation ◽

Archaeological Knowledge ◽

Burial Grounds

Ancient DNA from Yersinia pestis has been identified in skeletons at four urban burial grounds in Cambridge, England, and at a nearby rural cemetery. Dating to between ad 1349 and 1561, these represent individuals who died of plague during the second pandemic. Most come from normative individual burials, rather than mass graves. This pattern represents a major advance in archaeological knowledge, shifting focus away from a few exceptional discoveries of mass burials to what was normal practice in most medieval contexts. Detailed consideration of context allows the authors to identify a range of burial responses to the second pandemic within a single town and its hinterland. This permits the creation of a richer and more varied narrative than has previously been possible.

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Assessing the origins of the European Plagues following the Black Death: a synthesis of genomic, historical and ecological information

10.1101/2021.04.20.440561 ◽

2021 ◽

Author(s):

Barbara Bramanti ◽

Yarong Wu ◽

Ruifu Yang ◽

Yujun Cui ◽

Nils Chr. Stenseth

Keyword(s):

Yersinia Pestis ◽

Ancient Dna ◽

Black Death ◽

Holistic View ◽

Scientific Debate ◽

Ecological Information ◽

Scientific Disagreement ◽

Western European

AbstractThe Second Plague Pandemic started in Europe with the Black Death in 1346 and lasted until the 19th century. Based on ancient DNA studies, there is a scientific disagreement over whether the bacterium, Yersinia pestis, came into Europe once (Hypothesis 1), or repeatedly over the following four centuries (Hypothesis 2). Here we synthesize the most updated phylogeny together with historical, archeological, evolutionary and ecological information. On the basis of this holistic view, we conclude that Hypothesis 2 is the most plausible. We also suggest that Y. pestis lineages might have developed attenuated virulence during transmission, which can explain the convergent evolutionary signals, including pla-decay, that appeared at the end of the pandemics.Significance StatementOver the last few years there has been a great deal of scientific debate regarding whether the plague bacterium, Yersinia pestis, spread from a Western European reservoir during the Second Plague Pandemic, or if it repeatedly came to Europe from Asia. Here we make a synthesis of the available evidence, including genomes of ancient DNA, historical, archeological and ecological information. We conclude that the bacterium most likely came to Europe from Asia several times during the Second Plague Pandemic.

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Absence of Yersinia pestis-specific DNA in human teeth from five European excavations of putative plague victims

Microbiology ◽

10.1099/mic.0.26594-0 ◽

2004 ◽

Vol 150 (2) ◽

pp. 341-354 ◽

Cited By ~ 107

Author(s):

M. Thomas P. Gilbert ◽

Jon Cuccui ◽

William White ◽

Niels Lynnerup ◽

Richard W. Titball ◽

...

Keyword(s):

Yersinia Pestis ◽

Ancient Dna ◽

Dna Sequences ◽

Bacterial Species ◽

Collaborative Study ◽

Independent Research ◽

Human Teeth ◽

Bacterial Dna ◽

Embedding Technique ◽

Positive Results

This study reports the results of a collaborative study undertaken by two independent research groups to (a) confirm recent PCR-based detection of Yersinia pestis DNA in human teeth from medieval plague victims in France, and (b) to extend these observations over five different European burial sites believed to contain plague victims dating from the late 13th to 17th centuries. Several different sets of primers were used, including those previously documented to yield positive results on ancient DNA extracts. No Y. pestis DNA could be amplified from DNA extracted from 108 teeth belonging to 61 individuals, despite the amplification of numerous other bacterial DNA sequences. Several methods of extracting dentine prior to the DNA extraction were also compared. PCR for bacterial 16S rDNA indicated the presence of multiple bacterial species in 23 out of 27 teeth DNA extracts where dentine was extracted using previously described methods. In comparison, positive results were obtained from only five out of 44 teeth DNA extracts for which a novel contamination-minimizing embedding technique was used. Therefore, high levels of environmental bacterial DNA are present in DNA extracts where previously described methods of tooth manipulation are used. To conclude, the absence of Y. pestis-specific DNA in an exhaustive search using specimens from multiple putative European plague burial sites does not allow us to confirm the identification of Y. pestis as the aetiological agent of the Black Death and subsequent plagues. In addition, the utility of the published tooth-based ancient DNA technique used to diagnose fatal bacteraemias in historical epidemics still awaits independent corroboration.

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Implications of ancient DNA for phylogenetic studies

Cellular and Molecular Life Sciences ◽

10.1007/bf01921723 ◽

1994 ◽

Vol 50 (6) ◽

pp. 543-550 ◽

Cited By ~ 20

Author(s):

R. DeSalle

Keyword(s):

Ancient Dna ◽

Phylogenetic Studies

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Die Justinianische Pest

Evangelische Theologie ◽

10.14315/evth-2021-810509 ◽

2021 ◽

Vol 81 (5) ◽

pp. 385-401

Author(s):

Marcel Keller ◽

Christof Paulus ◽

Elena Xoplaki

Keyword(s):

Yersinia Pestis ◽

Crisis Management ◽

Focus Of Attention ◽

Integrative Approach ◽

Mutual Understanding ◽

Late Antique ◽

Causal Inferences ◽

Phylogenetic Studies ◽

Temporal Extent ◽

Written Sources

Abstract Of all known epidemics in Antiquity, the Justinianic Plague became the focus of attention in recent years - not least because it is the first for which the causative agent, the bacterium Yersinia pestis, could be unambiguously identified by palaeogeneticists. The reconstruction of ancient Y. pestis genomes is able to uncover the geographical and temporal extent of the pandemic beyond the limitations of written sources; and phylogenetic studies allow for inferences on the origin and spread of plague through time. But even the mere identification of plague victims in Late Antique and Early Medieval cemeteries offers insights in the crisis management and reactions of past societies to the irruption of the unfathomable, to which historical scholarship - generally based on written sources - has only limited access. However, attempts on the integration of natural scientific research on epidemics and climatic shifts in history are notoriously accused of determinism or an oversimplification of complex coherencies. Therefore, mutual understanding of methodologies and epistemologies of different disciplines is a fundamental prerequisite to avoid simplistic causal inferences from correlations and circular arguments, and lead to a better understanding of the Justinianic Plague and accompanying processes through an integrative approach.

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Assessing the origins of the European Plagues following the Black Death: A synthesis of genomic, historical, and ecological information

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2101940118 ◽

2021 ◽

Vol 118 (36) ◽

pp. e2101940118

Author(s):

Barbara Bramanti ◽

Yarong Wu ◽

Ruifu Yang ◽

Yujun Cui ◽

Nils Chr. Stenseth

Keyword(s):

Yersinia Pestis ◽

19Th Century ◽

Ancient Dna ◽

Black Death ◽

Holistic View ◽

Ecological Information ◽

Scientific Disagreement ◽

The 19Th Century

The second plague pandemic started in Europe with the Black Death in 1346 and lasted until the 19th century. Based on ancient DNA studies, there is a scientific disagreement over whether the bacterium, Yersinia pestis, came into Europe once (Hypothesis 1) or repeatedly over the following four centuries (Hypothesis 2). Here, we synthesize the most updated phylogeny together with historical, archeological, evolutionary, and ecological information. On the basis of this holistic view, we conclude that Hypothesis 2 is the most plausible. We also suggest that Y. pestis lineages might have developed attenuated virulence during transmission, which can explain the convergent evolutionary signals, including pla decay, that appeared at the end of the pandemics.

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