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Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America.

ABSTRACT: Yersinia pestis, the etiologic agent of plague, was responsible for several devastating epidemics throughout history and is currently of global importance to current public heath and biodefense efforts. Y. pestis is widespread in the Western United States. Because Y. pestis was first introduced to this region just over 100 years ago, there has been little time for genetic diversity to accumulate. Recent studies based upon single nucleotide polymorphisms have begun to quantify the genetic diversity of Y. pestis in North America.To examine the evolution of Y. pestis in North America, a gapped genome sequence of CA88-4125 was generated. Sequence comparison with another North American Y. pestis strain, CO92, identified seven regions of difference (six inversions, one rearrangement), differing IS element copy numbers, and several SNPs.The relatively large number of inverted/rearranged segments suggests that North American Y. pestis strains may be undergoing inversion fixation at high rates over a short time span, contributing to higher-than-expected diversity in this region. These findings will hopefully encourage the scientific community to sequence additional Y. pestis strains from North America and abroad, leading to a greater understanding of the evolutionary history of this pathogen.

SUBMITTER: Auerbach RK

PROVIDER: S-EPMC1940323 | biostudies-literature | 2007 Aug

REPOSITORIES: biostudies-literature

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Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America.

Auerbach Raymond K RK Tuanyok Apichai A Probert William S WS Kenefic Leo L Vogler Amy J AJ Bruce David C DC Munk Christine C Brettin Thomas S TS Eppinger Mark M Ravel Jacques J Wagner David M DM Keim Paul P

PloS one 20070822 8

<h4>Background</h4>Yersinia pestis, the etiologic agent of plague, was responsible for several devastating epidemics throughout history and is currently of global importance to current public heath and biodefense efforts. Y. pestis is widespread in the Western United States. Because Y. pestis was first introduced to this region just over 100 years ago, there has been little time for genetic diversity to accumulate. Recent studies based upon single nucleotide polymorphisms have begun to quantify ...[more]

PMID: 17712418

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Project description:The life cycle of Yersinia pestis has changed a lot to adapt to flea-borne transmission since it evolved from an enteric pathogen, Yersinia pseudotuberculosis. Small insertions and deletions (indels), especially frameshift mutations, can have major effects on phenotypes and contribute to virulence and host adaptation through gene disruption and inactivation. Here, we analyzed 365 Y. pestis genomes and identified 2,092 genome-wide indels on the core genome. As recently reported in Mycobacterium tuberculosis, we also detected "indel pockets" in Y. pestis, with average complexity scores declining around indel positions, which we speculate might also exist in other prokaryotes. Phylogenic analysis showed that indel-based phylogenic tree could basically reflect the phylogenetic relationships of major phylogroups in Y. pestis, except some inconsistency around the Big Bang polytomy. We observed 83 indels arising in the trunk of the phylogeny, which played a role in accumulation of pseudogenes related to key metabolism and putatively pathogenicity. We also discovered 32 homoplasies at the level of phylogroups and 7 frameshift scars (i.e., disrupted reading frame being rescued by a second frameshift). Additionally, our analysis showed evidence of parallel evolution at the level of genes, with sspA, rpoS, rnd, and YPO0624, having enriched mutations in Brazilian isolates, which might be advantageous for Y. pestis to cope with fluctuating environments. The diversified selection signals observed here demonstrates that indels are important contributors to the adaptive evolution of Y. pestis. Meanwhile, we provide potential targets for further exploration, as some genes/pseudogenes with indels we focus on remain uncharacterized. IMPORTANCE Yersinia pestis, the causative agent of plague, is a highly pathogenic clone of Yersinia pseudotuberculosis. Previous genome-wide SNP analysis provided few adaptive signatures during its evolution. Here by investigating 365 public genomes of Y. pestis, we give a comprehensive overview of general features of genome-wide indels on the core genome and their roles in Y. pestis evolution. Detection of "indel pockets," with average complexity scores declining around indel positions, in both Mycobacterium tuberculosis and Y. pestis, gives us a clue that this phenomenon might appear in other bacterial genomes. Importantly, the identification of four different forms of selection signals in indels would improve our understanding on adaptive evolution of Y. pestis, and provide targets for further physiological mechanism researches of this pathogen. As evolutionary research based on genome-wide indels is still rare in bacteria, our study would be a helpful reference in deciphering the role of indels in other species.

Dataset Information

Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America.

Publications

Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America.

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