Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity

Journal name:
Nature Genetics
Volume:
42,
Pages:
1140–1143
Year published:
DOI:
doi:10.1038/ng.705
Received
Accepted
Published online

Plague is a pandemic human invasive disease caused by the bacterial agent Yersinia pestis. We here report a comparison of 17 whole genomes of Y. pestis isolates from global sources. We also screened a global collection of 286 Y. 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 that Y. 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 of Y. pestis is marked by sequential, geographically specific SNPs.

At a glance

Figures

  1. Genomic maximum parsimony tree and divergence dates based on 1,364 non-repetitive, non-homoplastic SNPs from 3,349 coding sequences in 16 Y. pestis genomes (excluding FV-1).
    Figure 1: Genomic maximum parsimony tree and divergence dates based on 1,364 non-repetitive, non-homoplastic SNPs from 3,349 coding sequences in 16 Y. pestis genomes (excluding FV-1).

    Black text, names of genomic sequences (Supplementary Table 1); colored text, branch and population names; gray, ranges of maximal and minimal dates of divergence for individual branches calculated22 with strict mutation rates of 2.9 × 10−9 and 2.3 × 10−8 per site per year (Supplementary Table 2). Comparable results were obtained using intergenic SNPs or a variable clock rate (Supplementary Table 2b). ya, years ago.

  2. Fully parsimonious minimal spanning tree of 933 SNPs for 282 isolates of Y. pestis colored by location.
    Figure 2: Fully parsimonious minimal spanning tree of 933 SNPs for 282 isolates of Y. pestis colored by location.

    Large, bold text, branches 1, 2 and 0; smaller letters, populations (for example, 1.ORI3); lower case letters, nodes (for example, 1.ORI3.a). Strain designations near terminal nodes, genomic sequences. Roman numbers, hypothetical nodes. Gray text on lines between nodes, numbers of SNPs, except that one or two SNPs are indicated by thick and thin black lines, respectively. Six additional isolates in 0.PE1 and 0.PE2b (blue dashes) were tested only for selected, informative SNPs.

Accession codes

Referenced accessions

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References

  1. Linz, B. et al. An African origin for the intimate association between humans and Helicobacter pylori . Nature 445, 915918 (2007).
  2. Diamond, J. Guns, Germs and Steel 1480 (Jonathan Cape, London, UK, 1997).
  3. Stenseth, N.C. et al. Plague: past, present, and future. PLoS Med. 5, e3 (2008).
  4. Keeling, M.J. & Gilligan, C.A. Metapopulation dynamics of bubonic plague. Nature 407, 903906 (2000).
  5. Pollitzer, R. Plague studies. 1. A summary of the history and survey of the present distribution of the disease. Bull. World Health Organ. 4, 475533 (1951).
  6. Devignat, R. Variétés de l′espèce Pasteurella pestis. Nouvelle hypothèse. Bull. World Health Organ. 4, 247263 (1951).
  7. Wu, L.T. Chapter I: historical aspects. in Plague: A Manual for Medical and Public Health Workers 155 (Weishengshu, National Quarantine Service, Shanghai, China, 1936).
  8. Anisimov, A.P., Lindler, L.E. & Pier, G.B. Intraspecific diversity of Yersinia pestis . Clin. Microbiol. Rev. 17, 434464 (2004).
  9. Achtman, M. Evolution, population structure and phylogeography of genetically monomorphic bacterial pathogens. Annu. Rev. Microbiol. 62, 5370 (2008).
  10. Achtman, M. et al. Microevolution and history of the plague bacillus, Yersinia pestis . Proc. Natl. Acad. Sci. USA 101, 1783717842 (2004).
  11. Brygoo, E.R. Epidemiologie de la peste à Madagascar. Archive de l′lnstitut Pasteur de Madagascar 35, 7147 (1966).
  12. Girard, G. Immunity in plague. Acquisitions supplied by 30 years of work on the “Pasteurella pestis EV” (Girard and Robic) strain. Biol. Med. (Paris) 52, 631731 (1963).
  13. Li, Y. et al. Genotyping and phylogenetic analysis of Yersinia pestis by MLVA: insights into the worldwide expansion of Central Asia plague foci. PLoS ONE 4, e6000 (2009).
  14. Haensch, S. et al. Distinct clones of Yersinia pestis caused the Black Death. PLoS Pathog 6, e1001134 (2010).
  15. Silkroad Foundation. The Bridge between Eastern and Western Cultures. (2009)left fencehttp://www.silkroadfoundation.org/toc/index.htmlright fence.
  16. Levathes, L. When China Ruled the Seas: The Treasure Fleet of the Dragon Throne, 1405–1433 1252 (Oxford University Press, New York, 1996).
  17. Link, V.B. A history of plague in United States of America. Public Health Monogr. 26, 1120 (1955).
  18. Yu, H.L. & Christakos, G. Spatiotemporal modelling and mapping of the bubonic plague epidemic in India. Int. J. Health Geogr. 5, 12 (2006).
  19. Del Rio, A., Zegers, R., Boza, R.D. & Montero, L. Informe sobre la epidemia de peste bubonica. La Chilena di Hijiene IX, 17 (1904).
  20. Nocht, B. & Giemsa G. Ueber die Vernichtung von Ratten an Bord von Schiffen als Massregel gegen die Einschleppung der Pest. Arbeiten aus dem Kaiserlichen Gesundheitsamte XX, 6 (1903).
  21. Lauzeral, P. & Millischer, P. A propos de la filiation de deux cas. Bull. Soc. Pathol. Exot. 25, 935941 (1932).
  22. Drummond, A.J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).
  23. Adjemian, J.Z., Foley, P., Gage, K.L. & Foley, J.E. Initiation and spread of traveling waves of plague, Yersinia pestis, in the western United States. Am. J. Trop. Med. Hyg. 76, 365375 (2007).
  24. Guiyoule, A. et al. Recent emergence of new variants of Yersinia pestis in Madagascar. J. Clin. Microbiol. 35, 28262833 (1997).
  25. Zhou, D. et al. DNA microarray analysis of genome dynamics in Yersinia pestis: insights into bacterial genome microevolution and niche adaptation. J. Bacteriol. 186, 51385146 (2004).
  26. Eppinger, M. et al. Draft genome sequences of Yersinia pestis isolates from natural foci of endemic plague in China. J. Bacteriol. 191, 76287629 (2009).
  27. Eppinger, M. et al. Genome sequence of the deep-rooted Yersinia pestis strain Angola reveals new insights into the evolution and pangenome of the plague bacterium. J. Bacteriol. 192, 16851699 (2010).
  28. 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).
  29. Touchman, J.W. et al. A North American Yersinia pestis draft genome sequence: SNPs and phylogenetic analysis. PLoS ONE 2, e220 (2007).
  30. Garcia, E. et al. Pestoides F, an atypical Yersinia pestis strain from the former Soviet Union. Adv. Exp. Med. Biol. 603, 1722 (2007).
  31. Song, Y. et al. Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11, 179197 (2004).
  32. 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, 44534463 (2006).
  33. Parkhill, J. et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523527 (2001).
  34. Deng, W. et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184, 46014611 (2002).
  35. Chain, P.S.G. et al. Insights into the genome evolution of Yersinia pestis through whole genome comparison with Yersinia pseudotuberculosis . Proc. Natl. Acad. Sci. USA 101, 1382613831 (2004).
  36. Welch, T.J. et al. Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS ONE 2, e309 (2007).
  37. Galimand, M. et al. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 337, 677680 (1997).
  38. Pearson, T., Okinaka, R.T., Foster, J.T. & Keim, P. Phylogenetic understanding of clonal populations in an era of whole genome sequencing. Infect. Genet. Evol. 9, 10101019 (2009).
  39. Roumagnac, P. et al. Evolutionary history of Salmonella Typhi. Science 314, 13011304 (2006).
  40. Nelson, K.E. et al. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima . Nature 399, 323329 (1999).
  41. Eppinger, M. et al. The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative Agent of Far East scarlet-like fever. PLoS Genet. 3, e142 (2007).
  42. Huson, D.H. et al. Design of a compartmentalized shotgun assembler for the human genome. Bioinformatics 17 (Suppl 1), S132S139 (2001).
  43. Holt, K.E. et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat. Genet. 40, 987993 (2008).
  44. Lowder, B.V. et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus . Proc. Natl. Acad. Sci. USA 106, 1954519550 (2009).
  45. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
  46. Vogler, A.J. et al. Assays for the rapid and specific identification of North American Yersinia pestis and the common laboratory strain CO92. Biotechniques 44, 201 203–204, 207 (2008).
  47. Vogler, A.J. et al. Phylogeography of Francisella tularensis: global expansion of a highly fit clone. J. Bacteriol. 191, 24742484 (2009).

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Author information

  1. 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.).

    • Giovanna Morelli,
    • Yajun Song,
    • Camila J Mazzoni &
    • Mark Eppinger

Affiliations

  1. Max-Planck-Institut für Infektionsbiologie, Department of Molecular Biology, 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. Muséum National d′Histoire Naturelle–Ecole Pratique des Hautes Etudes, Department of Systematics and Evolution UMR-CNRS 7205, 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

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. contributed Y. 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.

Competing financial interests

The authors declare no competing financial interests.

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Supplementary information

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    Supplementary Figures 1–5, Supplementary Tables 1 and 2 and Supplementary Note

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