1887

Abstract

, the causative agent of plague, is best known for historical pandemics, but still actively causes disease in many parts of the world. is a recently derived clone of the pathogenic species , but is more associated with human infection. Numerous studies have documented genomic changes since the two species differentiated, although all of these studies used a relatively small sample set for defining these differences. In this study, we compared the complete genomic content between a diverse set of and genomes, and identified unique loci that could serve as diagnostic markers or for better understanding the evolution and pathogenesis of each group. Comparative genomics analyses also identified subtle variations in gene content between individual monophyletic clades within these species, based on a core genome single nucleotide polymorphism phylogeny that would have been undetected in a less comprehensive genome dataset. We also screened loci that were identified in other published studies as unique to either species and generally found a non-uniform distribution, suggesting that the assignment of these unique genes to either species should be re-evaluated in the context of current sequencing efforts. Overall, this study provides a high-resolution view into the genomic differences between and , demonstrating fine-scale differentiation and unique gene composition in both species.

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2015-08-03
2024-04-19
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References

  1. Achtman M. 2008; Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62:53–70 [View Article][PubMed]
    [Google Scholar]
  2. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. 1999; Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis . Proc Natl Acad Sci U S A 96:14043–14048 [View Article][PubMed]
    [Google Scholar]
  3. Achtman M., Morelli G., Zhu P., Wirth T., Diehl I., Kusecek B., Vogler A.J., Wagner D.M., Allender C.J. otherauthors 2004; Microevolution and history of the plague bacillus, Yersinia pestis . Proc Natl Acad Sci U S A 101:17837–17842 [View Article][PubMed]
    [Google Scholar]
  4. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  5. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. 1997; Gapped blast psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  6. Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S. otherauthors 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477 [View Article][PubMed]
    [Google Scholar]
  7. Benson D.A., Karsch-Mizrachi I., Clark K., Lipman D.J., Ostell J., Sayers E.W. 2012; GenBank. Nucleic Acids Res 40:(D1)D48–D53 [View Article][PubMed]
    [Google Scholar]
  8. Bonacorsi S.P., Scavizzi M.R., Guiyoule A., Amouroux J.H., Carniel E. 1994; Assessment of a fluoroquinolone, three beta-lactams, two aminoglycosides, and a cycline in treatment of murine Yersinia pestis infection. Antimicrob Agents Chemother 38:481–486 [View Article][PubMed]
    [Google Scholar]
  9. Brubaker R.R. 1991; Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev 4:309–324[PubMed]
    [Google Scholar]
  10. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K. otherauthors 2010; qiime allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336 [View Article][PubMed]
    [Google Scholar]
  11. Chain P.S., Carniel E., Larimer F.W., Lamerdin J., Stoutland P.O., Regala W.M., Georgescu A.M., Vergez L.M., Land M.L. otherauthors 2004; Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis . Proc Natl Acad Sci U S A 101:13826–13831 [View Article][PubMed]
    [Google Scholar]
  12. Chain P.S., Hu P., Malfatti S.A., Radnedge L., Larimer F., Vergez L.M., Worsham P., Chu M.C., Andersen G.L. 2006; Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J Bacteriol 188:4453–4463 [View Article][PubMed]
    [Google Scholar]
  13. Cui Y., Yu C., Yan Y., Li D., Li Y., Jombart T., Weinert L.A., Wang Z., Guo Z. otherauthors 2013; Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis . Proc Natl Acad Sci U S A 110:577–582 [View Article][PubMed]
    [Google Scholar]
  14. Delcher A.L., Salzberg S.L., Phillippy A.M. 2003; Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics 10:3.1–3.18
    [Google Scholar]
  15. DePristo M.A., Banks E., Poplin R., Garimella K.V., Maguire J.R., Hartl C., Philippakis A.A., del Angel G., Rivas M.A. otherauthors 2011; A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498 [View Article][PubMed]
    [Google Scholar]
  16. Derbise A., Carniel E. 2014; YpfΦ: a filamentous phage acquired by Yersinia pestis . Front Microbiol 5:701 [View Article][PubMed]
    [Google Scholar]
  17. Derbise A., Chenal-Francisque V., Pouillot F., Fayolle C., Prévost M.C., Médigue C., Hinnebusch B.J., Carniel E. 2007; A horizontally acquired filamentous phage contributes to the pathogenicity of the plague bacillus. Mol Microbiol 63:1145–1157 [View Article][PubMed]
    [Google Scholar]
  18. Duan R., Liang J., Shi G., Cui Z., Hai R., Wang P., Xiao Y., Li K., Qiu H. otherauthors 2014; Homology analysis of pathogenic Yersinia species Yersinia enterocolitica Yersinia pseudotuberculosis, and Yersinia pestis based on multilocus sequence typing. J Clin Microbiol 52:20–29 [View Article][PubMed]
    [Google Scholar]
  19. Edgar R.C. 2004; muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113 [View Article][PubMed]
    [Google Scholar]
  20. Edgar R.C. 2010; Search and clustering orders of magnitude faster than blast. Bioinformatics 26:2460–2461 [View Article][PubMed]
    [Google Scholar]
  21. Engelthaler D.M., Hicks N.D., Gillece J.D., Roe C.C., Schupp J.M., Driebe E.M., Gilgado F., Carriconde F., Trilles L. otherauthors 2014; Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. MBio 5:e01464–e01414 [View Article][PubMed]
    [Google Scholar]
  22. Farris J.S. 1989; The retention index and the rescaled consistency index. Cladistics 5:417–419 [View Article]
    [Google Scholar]
  23. Galimand M., Carniel E., Courvalin P. 2006; Resistance of Yersinia pestis to antimicrobial agents. Antimicrob Agents Chemother 50:3233–3236 [View Article][PubMed]
    [Google Scholar]
  24. Hu P., Elliott J., McCready P., Skowronski E., Garnes J., Kobayashi A., Brubaker R.R., Garcia E. 1998; Structural organization of virulence-associated plasmids of Yersinia pestis . J Bacteriol 180:5192–5202[PubMed]
    [Google Scholar]
  25. Hyatt D., Chen G.L., Locascio P.F., Land M.L., Larimer F.W., Hauser L.J. 2010; Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119 [View Article][PubMed]
    [Google Scholar]
  26. Kent W.J. 2002; blat - the blast-like alignment tool. Genome Res 12:656–664 [View Article][PubMed]
    [Google Scholar]
  27. Koskiniemi S., Lamoureux J.G., Nikolakakis K.C., t'Kint de Roodenbeke C., Kaplan M.D., Low D.A., Hayes C.S. 2013; Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci U S A 110:7032–7037 [View Article]
    [Google Scholar]
  28. Krzywinski M., Schein J., Birol I., Connors J., Gascoyne R., Horsman D., Jones S.J., Marra M.A. 2009; Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645 [View Article][PubMed]
    [Google Scholar]
  29. Letunic I., Bork P. 2007; Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128 [View Article][PubMed]
    [Google Scholar]
  30. Li H. 2013; Aligning sequence reads, clone sequences and assembly contigs with bwa-mem . http://arxiv.org/abs/1303.3997
    [Google Scholar]
  31. Li Y., Dai E., Cui Y., Li M., Zhang Y., Wu M., Zhou D., Guo Z., Dai X. otherauthors 2008; Different region analysis for genotyping Yersinia pestis isolates from China. PLoS One 3:e2166 [View Article][PubMed]
    [Google Scholar]
  32. Lillard J.W. Jr, Fetherston J.D., Pedersen L., Pendrak M.L., Perry R.D. 1997; Sequence and genetic analysis of the hemin storage (hms) system of Yersinia pestis . Gene 193:13–21 [View Article][PubMed]
    [Google Scholar]
  33. McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S. otherauthors 2010; The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303 [View Article][PubMed]
    [Google Scholar]
  34. Perry R.D., Fetherston J.D. 1997; Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev 10:35–66[PubMed]
    [Google Scholar]
  35. Pouillot F., Fayolle C., Carniel E. 2008; Characterization of chromosomal regions conserved in Yersinia pseudotuberculosis and lost by Yersinia pestis . Infect Immun 76:4592–4599 [View Article][PubMed]
    [Google Scholar]
  36. Quinlan A.R., Hall I.M. 2010; BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842 [View Article][PubMed]
    [Google Scholar]
  37. Radnedge L., Agron P.G., Worsham P.L., Andersen G.L. 2002; Genome plasticity in Yersinia pestis . Microbiology 148:1687–1698[PubMed]
    [Google Scholar]
  38. Rasko D.A., Myers G.S., Ravel J. 2005; Visualization of comparative genomic analyses by blast score ratio. BMC Bioinformatics 6:2 [View Article][PubMed]
    [Google Scholar]
  39. Rasko D.A., Rosovitz M.J., Myers G.S., Mongodin E.F., Fricke W.F., Gajer P., Crabtree J., Sebaihia M., Thomson N.R. otherauthors 2008; The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893 [View Article][PubMed]
    [Google Scholar]
  40. Ratovonjato J., Rajerison M., Rahelinirina S., Boyer S. 2014; Yersinia pestis in Pulex irritans fleas during plague outbreak, Madagascar. Emerg Infect Dis 20:1414–1415 [View Article][PubMed]
    [Google Scholar]
  41. Reuter S., Connor T.R., Barquist L., Walker D., Feltwell T., Harris S.R., Fookes M., Hall M.E., Petty N.K. otherauthors 2014; Parallel independent evolution of pathogenicity within the genus Yersinia . Proc Natl Acad Sci U S A 111:6768–6773 [View Article][PubMed]
    [Google Scholar]
  42. Rosqvist R., Bölin I., Wolf-Watz H. 1988; Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect Immun 56:2139–2143[PubMed]
    [Google Scholar]
  43. Sahl J.W., Caporaso J.G., Rasko D.A., Keim P. 2014; The large-scale blast score ratio (LS-BSR) pipeline: a method to rapidly compare genetic content between bacterial genomes. PeerJ 2:e332 [View Article][PubMed]
    [Google Scholar]
  44. Schliep K.P. 2011; phangorn: phylogenetic analysis in r. Bioinformatics 27:592–593 [View Article][PubMed]
    [Google Scholar]
  45. Schubert S., Rakin A., Karch H., Carniel E., Heesemann J. 1998; Prevalence of the “high-pathogenicity island” of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect Immun 66:480–485[PubMed]
    [Google Scholar]
  46. Sodeinde O.A., Subrahmanyam Y.V., Stark K., Quan T., Bao Y., Goguen J.D. 1992; A surface protease and the invasive character of plague. Science 258:1004–1007 [View Article][PubMed]
    [Google Scholar]
  47. Stamatakis A. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  48. Sun Y.C., Jarrett C.O., Bosio C.F., Hinnebusch B.J. 2014; Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis . Cell Host Microbe 15:578–586 [View Article][PubMed]
    [Google Scholar]
  49. Van Ert M.N., Easterday W.R., Huynh L.Y., Okinaka R.T., Hugh-Jones M.E., Ravel J., Zanecki S.R., Pearson T., Simonson T.S. otherauthors 2007; Global genetic population structure of Bacillus anthracis . PLoS One 2:e461 [View Article][PubMed]
    [Google Scholar]
  50. Wagner D.M., Runberg J., Vogler A.J., Lee J., Driebe E., Price L.B., Engelthaler D.M., Fricke W.F., Ravel J., Keim P. 2010; No resistance plasmid in Yersinia pestis, North America. Emerg Infect Dis 16:885–887 [View Article][PubMed]
    [Google Scholar]
  51. Wagner D.M., Klunk J., Harbeck M., Devault A., Waglechner N., Sahl J.W., Enk J., Birdsell D.N., Kuch M. otherauthors 2014; Yersinia pestis and the plague of Justinian 541-543 AD: a genomic analysis. Lancet Infect Dis 14:319–326 [View Article][PubMed]
    [Google Scholar]
  52. Waterhouse A.M., Procter J.B., Martin D.M., Clamp M., Barton G.J. 2009; Jalview Version 2 – a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191 [View Article][PubMed]
    [Google Scholar]
  53. Welch T.J., Fricke W.F., McDermott P.F., White D.G., Rosso M.L., Rasko D.A., Mammel M.K., Eppinger M., Rosovitz M.J. otherauthors 2007; Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One 2:e309 [View Article][PubMed]
    [Google Scholar]
  54. Zerbino D.R., Birney E. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 [View Article][PubMed]
    [Google Scholar]
  55. Cui, Y. et al. (2011). Sequence Read Archive: http://www.ncbi.nlm.nih.gov/Traces/sra/?study = SRP003808.
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