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Yersinia pestis strains from Latvia show depletion of the pla virulence gene at the end of the second plague pandemic

Susat, Julian, Bonczarowska, Joanna H., Pētersone-Gordina, Elīna, Immel, Alexander, Nebel, Almut, Gerhards, Guntis, Krause-Kyora, Ben·2020·Scientific Reports

Abstract

Ancient genomic studies have identified Yersinia pestis(Y. pestis) as the causative agent of the second plague pandemic (fourteenth–eighteenth century) that started with the Black Death (1,347–1,353). Most of the Y. pestis strains investigated from this pandemic have been isolated from western Europe, and not much is known about the diversity and microevolution of this bacterium in eastern European countries. In this study, we investigated human remains excavated from two cemeteries in Riga (Latvia). Historical evidence suggests that the burials were a consequence of plague outbreaks during the seventeenth century. DNA was extracted from teeth of 16 individuals and subjected to shotgun sequencing. Analysis of the metagenomic data revealed the presence of Y. pestis sequences in four remains, confirming that the buried individuals were victims of plague. In two samples,Y. pestis DNA coverage was sufficient for genome reconstruction. Subsequent phylogenetic analysis showed that the Riga strains fell within the diversity of the already known post-Black Death genomes. Interestingly, the two Latvian isolates did not cluster together. Moreover, we detected a drop in coverage of the pPCP1 plasmid region containing the pla gene. Further analysis indicated the presence of two pPCP1 plasmids, one with and one without the pla gene region, and only one bacterial chromosome, indicating that the same bacterium carried two distinct pPCP1 plasmids. In addition, we found the same pattern in the majority of previously published post-Black Death strains, but not in the Black Death strains. The pla gene is an important virulence factor for the infection of and transmission in humans. Thus, the spread of pla-depleted strains may, among other causes, have contributed to the disappearance of the second plague pandemic in eighteenth century Europe.

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Research works printed but not linked: 61

  1. Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015). · DOI
  2. Valtuena, A. A. et al. The Stone Age plague and its persistence in Europe. Curr. Biol. 27, 3683–3691 (2017). · DOI
  3. Spyrou, M. A. et al. Analysis of 3800-year old Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat. Commun. 9, 2234. https://doi.org/10.1038/s41467-018-04550-9 (2018). · DOI
  4. Rascovan, N. et al. Emergence and spread of basal lineages of Yersinia pestis during the Neolithic Decline. Cell 176, 295–305 (2019). · DOI
  5. Anisimov, A. P., Lindler, L. E. & Pier, G. B. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev. 17, 434–464 (2004). · DOI
  6. Gage, K. L. & Kosoy, M. Y. Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol. 50, 505–528 (2005). · DOI
  7. Roelle, J. E., Miller, B. J., Godbey, J. L. & Biggins, D. E. Recovery of the black-footed ferret progress and continuing challenges. US Geol. Surv. Sci. Invest. Rep. 5293, 213–231 (2006).
  8. Morelli, G. et al. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 42, 1140–1143 (2010). · DOI
  9. Ziegler, P. The Black Death (Harper Collins, New York, 1969).
  10. Bos, K. I. et al. 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 (2016). · DOI
  11. Byrne, J. P. Encyclopedia of the Black Death (ABC-CLIO, Santa Barbara, 2012). · DOI
  12. Napiersky, J. G. L. Bodeckers Chronik livländischer und rigascher Ereignisse [Bodecker’s chronicle of Livonian and Riga events] (in German) (Kymmel’s Buchhandlung, Riga, 1890).
  13. Petersone-Gordina, E., Roberts, C., Millard, A. R., Montgomery, J. & Gerhards, G. Dental disease and dietary isotopes of individuals from St Gertrude Church cemetery, Riga, Lativia. PLoS ONE 13, e0191757. https://doi.org/10.1371/journal.pone.0191757 (2018). · DOI
  14. John, T. A. Bubonic Plague in Early Modern Russia: Public Health and Urban Disaster (Oxford University Press, Oxford, 2003).
  15. Bos, K. I. et al. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506–510 (2011). · DOI · Paper page
  16. Cui, Y. et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl. Acad. Sci. USA 110, 577–582 (2013). · DOI
  17. Namouchi, A. et al. Integrative approach using Yersinia pestis genomes to revisit the historical landscape of plague during the Medieval Period. Proc. Natl. Acad. Sci. USA 115, E11790–E11797. https://doi.org/10.1073/pnas.1812865115 (2018). · DOI
  18. Spyrou, M. A. et al. Historical Y pestis genomes reveal the European Black Death as the source of ancient and modern plague pandemics. Cell Host Microbe 19, 874–881 (2016). · DOI
  19. Spyrou, M. A. et al. Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes. Nat. Commun. 10, 4470. https://doi.org/10.1038/s41467-019-12154-0 (2019). · DOI · Paper page
  20. Appleby, A. B. The disappearance of plague: a continuing puzzle. Econ. Hist. Rev. 33, 161–173 (1980). · DOI
  21. Lenski, R. E. Evolution of plague virulence. Nature 334, 473–474 (1988). · DOI
  22. Zimbler, D. L., Schroeder, J. A., Eddy, J. L. & Lathem, W. W. Early emergence of Yersinia pestis as a severe respiratory pathogen. Nat. Commun. 6, 7487. https://doi.org/10.1038/ncomms8487 (2015). · DOI
  23. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6, 80–92 (2012). · DOI · Paper page
  24. Dirks, R. et al. Social responses during severe food shortages and famine. Cur. Anthropol. 21, 21–44 (1980). · DOI
  25. Pīrangs, H. Rīgas kapsētas [Graveyards of Riga] (in Latvian) (Rīgas pilsētas valde, Riga, 1932).
  26. Rusovs, B. Livonijas kronika [Chronicle of Livonia] (in Latvian) (Valters un Rapa, Riga, 1926).
  27. Degen, J. L., Bugge, T. H. & Goguen, J. D. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 5, 24–31 (2007). · DOI
  28. Lathem, W. W. et al. Post-transcriptional regulation of the Yersinia pestis cAMP receptor protein Crp and impact on virulence. MBio 5, e01038-13. https://doi.org/10.1128/mBio.01038-13 (2014). · DOI
  29. Perry, R. D. & Fetherston, J. D. Yersinia pestis—etiologic agent of plague. Clin. Microbiol. Rev. 10, 35–66 (1997). · DOI
  30. Sebbane, F., Jarrett, C. O., Gardner, D., Long, D. & Hinnebusch, B. J. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad. Sci. USA 103, 5526–5530 (2006). · DOI
  31. Sebbane, F. et al. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA 103, 11766–11771 (2006). · DOI
  32. Zhou, D. & Yang, R. Molecular Darwinian evolution of virulence in Yersinia pestis. Infect. Immun. 77, 2242–2250 (2009). · DOI
  33. Sun, Y. C., Jarret, C. O., Bosio, C. F. & Hinnebusch, B. J. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe 15, 578–584 (2014). · DOI
  34. Cavalcanti, Y. V. N., Leal, N. C. & De Almeida, A. M. P. Typing of Yersinia pestis isolates from the state of Ceará, Brazil. Lett. Appl. Microbiol. 35, 543–547 (2002). · DOI
  35. Filippov, A. A., Solodovnikov, N. S., Kookleva, L. M. & Protsenko, O. A. Plasmid content in Yersinia pestis strains of different origin. FEMS. Microbiol. Lett. 67, 45–48 (1990). · DOI
  36. Garcia, E. et al. Pestoides F, an atypical Yersinia pestis strain from the former Soviet Union. Adv. Exp. Med. Biol. 603, 17–22 (2007). · DOI
  37. Achtman, M. et al. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. USA 101, 17837–17842 (2004). · DOI
  38. Rajanna, C. et al. Characterization of pPCP1 plasmids in Yersinia pestis strains isolated from the former Soviet Union. Int. J. Microbiol. https://doi.org/10.1155/2010/760819 (2010). · DOI
  39. Gueneau de Novoa, P. & Williams, K. P. The tmRNA website: reductive evolution of tmRNA in plastids and other endosymbionts. Nucl. Acids. Res. 32, D104–D108. https://doi.org/10.1093/nar/gkh102 (2004). · DOI
  40. Keiler, K. C. Biology of trans-translation. Annu. Rev. Microbiol. 62, 133–151 (2008). · DOI
  41. Dulebohn, D., Choy, J., Sundermeier, T., Okan, N. & Karzai, A. W. Trans-translation: the tmRNA-mediated surveillance mechanism for ribosome rescue, directed protein degradation, and nonstop mRNA decay. Biochemistry 46, 4681–4693 (2007). · DOI
  42. Okan, N. A., Bliska, J. B. & Karzai, A. W. A role for the SmpB-SsrA system in Yersinia pseudotuberculosis pathogenesis. PLoS Pathog. 2, e6. https://doi.org/10.1371/journal.ppat.0020006 (2006). · DOI
  43. Baumler, A. J., Kusters, J. G., Stojiljkovic, I. & Heffron, F. Salmonella typhimurium loci involved in survival within macrophages. Infect. Immun. 62, 1623–1630 (1994). · DOI
  44. Julio, S. M., Heithoff, D. M. & Mahan, M. J. ssrA (tmRNA) plays a role in Salmonella enterica serovar Typhimurium pathogenesis. J. Bacteriol. 182, 1558–1563 (2000). · DOI
  45. Okan, N. A., Mena, P., Benach, J. L., Bliska, J. B. & Karzai, A. W. The smpB-ssrA mutant of Yersinia pestis functions as a live attenuated vaccine to protect mice against pulmonary plague infection. Infect. Immun. 78, 1284–1293 (2010). · DOI
  46. Petersone-Gordina, E., et al. Investigating dietary life histories and mobility in children buried in St Gertrude Church cemetery, Riga, Latvia (15th–17th centuries AD). Archaeometry 62, 3–18 (2020). · DOI
  47. Krause-Kyora, B. et al. Ancient DNA study reveals HLA susceptibility locus for leprosy in medieval Europeans. Nat. Commun. 9, 1569. https://doi.org/10.1038/s41467-018-03857-x (2018). · DOI
  48. Vågene, Å. J. et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nat. Ecol. Evol. 2, 520–528 (2018). · DOI
  49. Huson, D. H., Auch, A. F., Qi, J. & Schuster, S. C. MEGAN analysis of metagenomic data. Genome Res. 17, 377–386 (2007). · DOI
  50. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009). · DOI · Paper page
  51. Peltzer, A. et al. EAGER: efficient ancient genome reconstruction. Genome Biol. 17, 60. https://doi.org/10.1186/s13059-016-0918-z (2016). · DOI · Paper page
  52. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009). · DOI · Paper page
  53. McKenna, A. et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010). · DOI · Paper page
  54. Bos, K. I. et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014). · DOI · Paper page
  55. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). · DOI · Paper page
  56. Ronquist, F. et al. Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012). · DOI
  57. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001). · DOI · Paper page
  58. Briggs, A. W. et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc. Natl. Acad. Sci. USA 104, 14616–14621 (2007). · DOI · Paper page
  59. Lamnidis, T. C. et al. Ancient Fennoscandian genomes reveal origin and spread of Siberian ancestry in Europe. Nat. Commun. 9, 5018. https://doi.org/10.1038/s41467-018-07483-5 (2018). · DOI
  60. Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190. https://doi.org/10.1371/journal.pgen.0020190 (2006). · DOI · Paper page
  61. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009). · DOI · Paper page

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  • Ancient DNA analysis

    Orlando, L., Allaby, R., Skoglund, P., Der Sarkissian, C., Stockhammer, P. W., Ávila-Arcos, M. C., Fu, Q., Krause, J., Willerslev, E., Stone, A. C., et al. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-020-00011-0 · Cited by 411

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Metadata

Authors
Susat, J., Bonczarowska, J. H., Pētersone-Gordina, E., Immel, A., Nebel, A., Gerhards, G., & Krause-Kyora, B.
Venue
Scientific Reports
Published
2020-09-03
Volume
10
Issue
1
ISSN
2045-2322
Cited by
53
References
5
Language
en
Funders
  • Deutsche Forschungsgemeinschaft (2901391021 (CRC 1266))
  • Projekt DEAL

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