Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis

doi:10.1073/pnas.0404012101

Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis

^*Biology and Biotechnology Research Program, Lawrence Livermore National Laboratory, Livermore, CA 94550; ^†Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; ^‡Life Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831; ^§Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824; ^¶Rocky Mountain Laboratories, Hamilton, MT 59840; ^∥Institut National de la Santé etdela Recherche Médicale E0364, Université de Lille 2, Institut Pasteur de Lille, F-59021 Lille, France; and ^**Genoscope/Centre National de la Recherche Scientifique-Unité Mixte de Recherche 8030, 91006 Evry Cedex, France

Edited by Stanley Falkow, Stanford University, Stanford, CA, and approved August 4, 2004 (received for review June 5, 2004)

Abstract

Yersinia pestis, the causative agent of plague, is a highly uniform clone that diverged recently from the enteric pathogen Yersinia pseudotuberculosis. Despite their close genetic relationship, they differ radically in their pathogenicity and transmission. Here, we report the complete genomic sequence of Y. pseudotuberculosis IP32953 and its use for detailed genome comparisons with available Y. pestis sequences. Analyses of identified differences across a panel of Yersinia isolates from around the world reveal 32 Y. pestis chromosomal genes that, together with the two Y. pestis-specific plasmids, to our knowledge, represent the only new genetic material in Y. pestis acquired since the the divergence from Y. pseudotuberculosis. In contrast, 149 other pseudogenes (doubling the previous estimate) and 317 genes absent from Y. pestis were detected, indicating that as many as 13% of Y. pseudotuberculosis genes no longer function in Y. pestis. Extensive insertion sequence-mediated genome rearrangements and reductive evolution through massive gene loss, resulting in elimination and modification of preexisting gene expression pathways, appear to be more important than acquisition of genes in the evolution of Y. pestis. These results provide a sobering example of how a highly virulent epidemic clone can suddenly emerge from a less virulent, closely related progenitor.

Footnotes

↵ †† To whom correspondence should be addressed at: Lawrence Livermore National Laboratory, 7000 East Avenue, L-452, Livermore, CA, 94550. E-mail: garcia12{at}llnl.gov.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations: IS, insertion sequence; A, Antiqua; M, Medievalis; O, Orientalis; COG, Clusters of Orthologous Groups.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. BX936398 (chromosome), BX936399 (pYV), and BX936400 (pYptb32953)].