Parallel independent evolution of pathogenicity within the genus Yersinia

Sandra Reuter; Thomas R Connor; Lars Barquist; Danielle Walker; Theresa Feltwell; Simon R Harris; Maria Fookes; Miquette E Hall; Nicola K Petty; Thilo M Fuchs; Jukka Corander; Muriel Dufour; Tamara Ringwood; Cyril Savin; Christiane Bouchier; Liliane Martin; Minna Miettinen; Mikhail Shubin; Julia M Riehm; Riikka Laukkanen-Ninios; Leila M Sihvonen; Anja Siitonen; Mikael Skurnik; Juliana Pfrimer Falcão; Hiroshi Fukushima; Holger C Scholz; Michael B Prentice; Brendan W Wren; Julian Parkhill; Elisabeth Carniel; Mark Achtman; Alan McNally; Nicholas R Thomson

doi:10.1073/pnas.1317161111

Parallel independent evolution of pathogenicity within the genus Yersinia

Sandra Reuter, Thomas R Connor, Lars Barquist, Danielle Walker, Theresa Feltwell, Simon R Harris, Maria Fookes, Miquette E Hall, Nicola K Petty, Thilo M Fuchs, Jukka Corander, Muriel Dufour, Tamara Ringwood, Cyril Savin, Christiane Bouchier, Liliane Martin, Minna Miettinen, Mikhail Shubin, Julia M Riehm, Riikka Laukkanen-NiniosLeila M Sihvonen, Anja Siitonen, Mikael Skurnik, Juliana Pfrimer Falcão, Hiroshi Fukushima, Holger C Scholz, Michael B Prentice, Brendan W Wren, Julian Parkhill, Elisabeth Carniel, Mark Achtman, Alan McNally, Nicholas R Thomson

Microbiology and Infection

Research output: Contribution to journal › Article › peer-review

94 Citations (Scopus)

Abstract

The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.

Original language	English
Pages (from-to)	6768-6773
Number of pages	6
Journal	National Academy of Sciences. Proceedings
Volume	111
Issue number	18
Early online date	21 Apr 2014
DOIs	https://doi.org/10.1073/pnas.1317161111
Publication status	Published - 6 May 2014

Keywords

Evolution, Molecular
Genome, Bacterial
Humans
Metabolic Networks and Pathways
Phylogeny
Species Specificity
Virulence
Yersinia
Yersinia enterocolitica
genomics metabolic streamlining
pathoadaptation
Enterobacteriaceae

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Reuter, S., Connor, T. R., Barquist, L., Walker, D., Feltwell, T., Harris, S. R., Fookes, M., Hall, M. E., Petty, N. K., Fuchs, T. M., Corander, J., Dufour, M., Ringwood, T., Savin, C., Bouchier, C., Martin, L., Miettinen, M., Shubin, M., Riehm, J. M., ... Thomson, N. R. (2014). Parallel independent evolution of pathogenicity within the genus Yersinia. National Academy of Sciences. Proceedings, 111(18), 6768-6773. Advance online publication. https://doi.org/10.1073/pnas.1317161111

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title = "Parallel independent evolution of pathogenicity within the genus Yersinia",

abstract = "The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.",

keywords = "Evolution, Molecular, Genome, Bacterial, Humans, Metabolic Networks and Pathways, Phylogeny, Species Specificity, Virulence, Yersinia, Yersinia enterocolitica, genomics metabolic streamlining, pathoadaptation, Enterobacteriaceae",

author = "Sandra Reuter and Connor, {Thomas R} and Lars Barquist and Danielle Walker and Theresa Feltwell and Harris, {Simon R} and Maria Fookes and Hall, {Miquette E} and Petty, {Nicola K} and Fuchs, {Thilo M} and Jukka Corander and Muriel Dufour and Tamara Ringwood and Cyril Savin and Christiane Bouchier and Liliane Martin and Minna Miettinen and Mikhail Shubin and Riehm, {Julia M} and Riikka Laukkanen-Ninios and Sihvonen, {Leila M} and Anja Siitonen and Mikael Skurnik and Falc{\~a}o, {Juliana Pfrimer} and Hiroshi Fukushima and Scholz, {Holger C} and Prentice, {Michael B} and Wren, {Brendan W} and Julian Parkhill and Elisabeth Carniel and Mark Achtman and Alan McNally and Thomson, {Nicholas R}",

year = "2014",

month = may,

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doi = "10.1073/pnas.1317161111",

language = "English",

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journal = "National Academy of Sciences. Proceedings",

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Reuter, S, Connor, TR, Barquist, L, Walker, D, Feltwell, T, Harris, SR, Fookes, M, Hall, ME, Petty, NK, Fuchs, TM, Corander, J, Dufour, M, Ringwood, T, Savin, C, Bouchier, C, Martin, L, Miettinen, M, Shubin, M, Riehm, JM, Laukkanen-Ninios, R, Sihvonen, LM, Siitonen, A, Skurnik, M, Falcão, JP, Fukushima, H, Scholz, HC, Prentice, MB, Wren, BW, Parkhill, J, Carniel, E, Achtman, M, McNally, A & Thomson, NR 2014, 'Parallel independent evolution of pathogenicity within the genus Yersinia', National Academy of Sciences. Proceedings, vol. 111, no. 18, pp. 6768-6773. https://doi.org/10.1073/pnas.1317161111

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T1 - Parallel independent evolution of pathogenicity within the genus Yersinia

AU - Reuter, Sandra

AU - Connor, Thomas R

AU - Barquist, Lars

AU - Walker, Danielle

AU - Feltwell, Theresa

AU - Harris, Simon R

AU - Fookes, Maria

AU - Hall, Miquette E

AU - Petty, Nicola K

AU - Fuchs, Thilo M

AU - Corander, Jukka

AU - Dufour, Muriel

AU - Ringwood, Tamara

AU - Savin, Cyril

AU - Bouchier, Christiane

AU - Martin, Liliane

AU - Miettinen, Minna

AU - Shubin, Mikhail

AU - Riehm, Julia M

AU - Laukkanen-Ninios, Riikka

AU - Sihvonen, Leila M

AU - Siitonen, Anja

AU - Skurnik, Mikael

AU - Falcão, Juliana Pfrimer

AU - Fukushima, Hiroshi

AU - Scholz, Holger C

AU - Prentice, Michael B

AU - Wren, Brendan W

AU - Parkhill, Julian

AU - Carniel, Elisabeth

AU - Achtman, Mark

AU - McNally, Alan

AU - Thomson, Nicholas R

PY - 2014/5/6

Y1 - 2014/5/6

N2 - The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.

AB - The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.

KW - Evolution, Molecular

KW - Genome, Bacterial

KW - Humans

KW - Metabolic Networks and Pathways

KW - Phylogeny

KW - Species Specificity

KW - Virulence

KW - Yersinia

KW - Yersinia enterocolitica

KW - genomics metabolic streamlining

KW - pathoadaptation

KW - Enterobacteriaceae

U2 - 10.1073/pnas.1317161111

DO - 10.1073/pnas.1317161111

M3 - Article

C2 - 24753568

SN - 1091-6490

VL - 111

SP - 6768

EP - 6773

JO - National Academy of Sciences. Proceedings

JF - National Academy of Sciences. Proceedings

IS - 18

ER -

Parallel independent evolution of pathogenicity within the genus Yersinia

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Keywords

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