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Nature Genetics
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Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity

Nature Geneticsvolume 42, pages1140–1143 (2010)Cite this article

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Abstract

Plague is a pandemic human invasive disease caused by the bacterial agentYersinia pestis. We here report a comparison of 17 whole genomes ofY. pestis isolates from global sources. We also screened a global collection of 286Y. pestis isolates for 933 SNPs using Sequenom MassArray SNP typing. We conducted phylogenetic analyses on this sequence variation dataset, assigned isolates to populations based on maximum parsimony and, from these results, made inferences regarding historical transmission routes. Our phylogenetic analysis suggests thatY. pestis evolved in or near China and spread through multiple radiations to Europe, South America, Africa and Southeast Asia, leading to country-specific lineages that can be traced by lineage-specific SNPs. All 626 current isolates from the United States reflect one radiation, and 82 isolates from Madagascar represent a second radiation. Subsequent local microevolution ofY. pestis is marked by sequential, geographically specific SNPs.

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Figure 1: Genomic maximum parsimony tree and divergence dates based on 1,364 non-repetitive, non-homoplastic SNPs from 3,349 coding sequences in 16Y. pestis genomes (excluding FV-1).
Figure 2: Fully parsimonious minimal spanning tree of 933 SNPs for 282 isolates ofY. pestis colored by location.

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Acknowledgements

We gratefully acknowledge technical assistance by R. Nera and A. Doyle and helpful comments from A. Rambaut and D. Falush. Support was provided by grants from the German Army Medical Corps (MSAB15A013) and the Science Foundation of Ireland (05/FE1/B882) to M.A., the National Key Program for Infectious Diseases of China (2008ZX10004-009) and the State Key Development Program for Basic Research of China (2009CB522600) to R.Y. and the US Department of Homeland Security (NBCH2070001; HSHQDC-08-C00158) and US National Institutes of Health (AI065359) to P.K. and D.M.W. Whole genome sequencing ofY. pestis strains IP275, MG05-1020 and UG05-045 was supported by federal funds from the National Institute of Allergy and Infectious Diseases, US National Institutes of Health, Department of Health and Human Services (N01 AI-30071), and sequencing of IP674 was supported by funding for Sanger Institute Pathogen Genomics by the Wellcome Trust. Genomic DNA ofY. pestis MG05-1020 was kindly provided by S. Bearden and M. Schriefer (Centers for Disease Control and Prevention, Fort Collins, Colorado, USA).

Author information

Author notes

  1. Giovanna Morelli, Yajun Song, Camila J Mazzoni & Mark Eppinger

    Present address: These authors contributed equally to this work. Present addresses: Max-Planck-Institut für molekulare Genetik, Berlin, Germany (G.M. and B.K.), Berlin Center for Genomics in Biodiversity Research, Berlin, Germany (C.J.M.) and Max-Delbrück-Centrum für molekulare Medizin (MDC) Berlin-Buch, Berlin, Germany (M.F.).,

Authors and Affiliations

  1. Department of Molecular Biology, Max-Planck-Institut für Infektionsbiologie, Berlin, Germany

    Giovanna Morelli, Camila J Mazzoni, Philippe Roumagnac, Mirjam Feldkamp, Barica Kusecek, Thierry Wirth & Mark Achtman

  2. State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China

    Yajun Song, Yanjun Li, Yujun Cui & Ruifu Yang

  3. Environmental Research Institute, University College Cork, Cork, Ireland

    Yajun Song, Camila J Mazzoni & Mark Achtman

  4. Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA

    Mark Eppinger & Jacques Ravel

  5. Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Mixte Research Unit Biology and Genetics of Plant/Pathogen Interactions (UMR BGPI), Montpellier, France

    Philippe Roumagnac

  6. Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA

    David M Wagner, Amy J Vogler & Paul Keim

  7. The Wellcome Trust Sanger Institute, The Wellcome Trust Genome Campus, Hinxton, Cambridge, UK

    Nicholas R Thomson

  8. Medical Research Council (MRC) Centre for Outbreak Analysis and Modeling, Imperial College Faculty of Medicine, London, UK

    Thibaut Jombart & Francois Balloux

  9. Department of Systematics and Evolution UMR-CNRS 7205, Muséum National d′Histoire Naturelle–Ecole Pratique des Hautes Etudes, Paris, France

    Raphael Leblois & Thierry Wirth

  10. Institute of Human Genetics, German Research Center for Environmental Health, Neuherberg, Germany

    Peter Lichtner

  11. Unité Peste, Institut Pasteur de Madagascar, Madagascar

    Lila Rahalison

  12. Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado, USA

    Jeannine M Petersen

  13. Pathogen Genomics Division, Translational Genomics Research Institute, Phoenix, Arizona, USA

    Paul Keim

  14. Institut Pasteur, Yersinia Research Unit, Paris, France

    Elisabeth Carniel

  15. Department of Microbiology, University College Cork, Cork, Ireland

    Mark Achtman

Authors
  1. Giovanna Morelli

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  2. Yajun Song

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  3. Camila J Mazzoni

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  4. Mark Eppinger

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  5. Philippe Roumagnac

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  6. David M Wagner

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  7. Mirjam Feldkamp

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  8. Barica Kusecek

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  9. Amy J Vogler

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  10. Yanjun Li

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  11. Yujun Cui

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  12. Nicholas R Thomson

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  13. Thibaut Jombart

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  14. Raphael Leblois

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  15. Peter Lichtner

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  16. Lila Rahalison

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  17. Jeannine M Petersen

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  18. Francois Balloux

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  19. Paul Keim

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  20. Thierry Wirth

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  21. Jacques Ravel

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  22. Ruifu Yang

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  23. Elisabeth Carniel

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  24. Mark Achtman

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Contributions

M.A., T.W., D.M.W., P.R., J.R., R.Y. and P.K. designed the study. L.R., J.M.P., R.Y. and E.C. contributedY. pestis DNA and demographic information. G.M., Y.S., M.E., P.R., M.F., B.K., A.J.V., Y.L., Y.C., P.L. and N.R.T. performed sequencing, SNP discovery, MassArray and SNP testing. G.M., Y.S., C.J.M., M.E., P.R., D.M.W. and P.L. performed bioinformatic analyses of the data. C.J.M., T.J., R.L., F.B. and T.W. performed population genetic analyses. M.A., C.J.M., M.E., P.R., D.M.W., T.J., F.B., P.K., T.W., J.R., R.Y. and E.C. wrote the manuscript.

Corresponding authors

Correspondence toRuifu Yang,Elisabeth Carniel orMark Achtman.

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The authors declare no competing financial interests.

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Morelli, G., Song, Y., Mazzoni, C.et al.Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity.Nat Genet42, 1140–1143 (2010). https://doi.org/10.1038/ng.705

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