Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus

  1. Kirsten I Bos
  2. Alexander Herbig
  3. Jason Sahl
  4. Nicholas Waglechner
  5. Mathieu Fourment
  6. Stephen A Forrest
  7. Jennifer Klunk
  8. Verena J Schuenemann
  9. Debi Poinar
  10. Melanie Kuch
  11. G Brian Golding
  12. Olivier Dutour
  13. Paul Keim
  14. David M Wagner
  15. Edward C Holmes
  16. Johannes Krause  Is a corresponding author
  17. Hendrik N Poinar
  1. University of Tübingen, Germany
  2. Northern Arizona University, United States
  3. McMaster University, Canada
  4. The University of Sydney, Australia
  5. Université Bordeaux, France

Abstract

The 14th-18th century pandemic of Yersinia pestis caused devastating disease outbreaks in Europe for almost 400 years. The reasons for plague's persistence and abrupt disappearance in Europe are poorly understood, but could have been due to either the presence of now-extinct plague foci in Europe itself, or successive disease introductions from other locations. Here we present five Y. pestis genomes from one of the last European outbreaks of plague, from 1722 in Marseille, France. The lineage identified has not been found in any extant Y. pestis foci sampled to date, and has its ancestry in strains obtained from victims of the 14th century Black Death. These data suggest the existence of a previously uncharacterized historical plague focus that persisted for at least three centuries. We propose that this disease source may have been responsible for the many resurgences of plague in Europe following the Black Death.

Article and author information

Author details

  1. Kirsten I Bos

    Department of Archeological Sciences, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexander Herbig

    Department of Archeological Sciences, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Jason Sahl

    Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicholas Waglechner

    Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Mathieu Fourment

    Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Stephen A Forrest

    Department of Archeological Sciences, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Jennifer Klunk

    McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Verena J Schuenemann

    Department of Archeological Sciences, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Debi Poinar

    McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  10. Melanie Kuch

    McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. G Brian Golding

    Department of Biology, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  12. Olivier Dutour

    Laboratoire d'anthropologie biologique Paul Broca, Ecole Pratique des Hautes Etudes, PACEA, Université Bordeaux, Bordeaux, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Paul Keim

    Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. David M Wagner

    Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Edward C Holmes

    Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  16. Johannes Krause

    Department of Archeological Sciences, University of Tübingen, Tübingen, Germany
    For correspondence
    johannes.krause@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
  17. Hendrik N Poinar

    Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, Canada
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Richard A Neher, Max Planck Institute for Developmental Biology, Germany

Publication history

  1. Received: November 12, 2015
  2. Accepted: January 19, 2016
  3. Accepted Manuscript published: January 21, 2016 (version 1)
  4. Version of Record published: March 11, 2016 (version 2)

Copyright

© 2016, Bos et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kirsten I Bos
  2. Alexander Herbig
  3. Jason Sahl
  4. Nicholas Waglechner
  5. Mathieu Fourment
  6. Stephen A Forrest
  7. Jennifer Klunk
  8. Verena J Schuenemann
  9. Debi Poinar
  10. Melanie Kuch
  11. G Brian Golding
  12. Olivier Dutour
  13. Paul Keim
  14. David M Wagner
  15. Edward C Holmes
  16. Johannes Krause
  17. Hendrik N Poinar
(2016)
Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus
eLife 5:e12994.
https://doi.org/10.7554/eLife.12994

Further reading

  1. DNA from 18th century teeth reveals plague secrets.

    1. Epidemiology and Global Health
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    Fabrizio Menardo
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    Detecting factors associated with transmission is important to understand disease epidemics, and to design effective public health measures. Clustering and terminal branch lengths (TBL) analyses are commonly applied to genomic data sets of Mycobacterium tuberculosis (MTB) to identify sub-populations with increased transmission. Here, I used a simulation-based approach to investigate what epidemiological processes influence the results of clustering and TBL analyses, and whether differences in transmission can be detected with these methods. I simulated MTB epidemics with different dynamics (latency, infectious period, transmission rate, basic reproductive number R0, sampling proportion, sampling period, and molecular clock), and found that all considered factors, except for the length of the infectious period, affect the results of clustering and TBL distributions. I show that standard interpretations of this type of analyses ignore two main caveats: (1) clustering results and TBL depend on many factors that have nothing to do with transmission, (2) clustering results and TBL do not tell anything about whether the epidemic is stable, growing, or shrinking, unless all the additional parameters that influence these metrics are known, or assumed identical between sub-populations. An important consequence is that the optimal SNP threshold for clustering depends on the epidemiological conditions, and that sub-populations with different epidemiological characteristics should not be analyzed with the same threshold. Finally, these results suggest that different clustering rates and TBL distributions, that are found consistently between different MTB lineages, are probably due to intrinsic bacterial factors, and do not indicate necessarily differences in transmission or evolutionary success.