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.
authors.affiliation: Pathogen Research Group, Nottingham Trent University, Nottingham NG11 8NS, United Kingdom.
authors.forename: Sandra
authors.initials: S
authors.lastname: Reuter
authors.forename: Thomas R
authors.initials: TR
authors.lastname: Connor
authors.forename: Lars
authors.initials: L
authors.lastname: Barquist
authors.forename: Danielle
authors.initials: D
authors.lastname: Walker
authors.forename: Theresa
authors.initials: T
authors.lastname: Feltwell
authors.forename: Simon R
authors.initials: SR
authors.lastname: Harris
authors.forename: Maria
authors.initials: M
authors.lastname: Fookes
authors.forename: Miquette E
authors.initials: ME
authors.lastname: Hall
authors.forename: Nicola K
authors.initials: NK
authors.lastname: Petty
authors.forename: Thilo M
authors.initials: TM
authors.lastname: Fuchs
authors.forename: Jukka
authors.initials: J
authors.lastname: Corander
authors.forename: Muriel
authors.initials: M
authors.lastname: Dufour
authors.forename: Tamara
authors.initials: T
authors.lastname: Ringwood
authors.forename: Cyril
authors.initials: C
authors.lastname: Savin
authors.forename: Christiane
authors.initials: C
authors.lastname: Bouchier
authors.forename: Liliane
authors.initials: L
authors.lastname: Martin
authors.forename: Minna
authors.initials: M
authors.lastname: Miettinen
authors.forename: Mikhail
authors.initials: M
authors.lastname: Shubin
authors.forename: Julia M
authors.initials: JM
authors.lastname: Riehm
authors.forename: Riikka
authors.initials: R
authors.lastname: Laukkanen-Ninios
authors.forename: Leila M
authors.initials: LM
authors.lastname: Sihvonen
authors.forename: Anja
authors.initials: A
authors.lastname: Siitonen
authors.forename: Mikael
authors.initials: M
authors.lastname: Skurnik
authors.forename: Juliana Pfrimer
authors.initials: JP
authors.lastname: Falcão
authors.forename: Hiroshi
authors.initials: H
authors.lastname: Fukushima
authors.forename: Holger C
authors.initials: HC
authors.lastname: Scholz
authors.forename: Michael B
authors.initials: MB
authors.lastname: Prentice
authors.forename: Brendan W
authors.initials: BW
authors.lastname: Wren
authors.forename: Julian
authors.initials: J
authors.lastname: Parkhill
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Carniel
authors.forename: Mark
authors.initials: M
authors.lastname: Achtman
authors.forename: Alan
authors.initials: A
authors.lastname: McNally
authors.forename: Nicholas R
authors.initials: NR
authors.lastname: Thomson
mesh_terms: D019143:Evolution, Molecular; D016680:Genome, Bacterial; D006801:Humans; D053858:Metabolic Networks and Pathways / Q000235:genetics; D010802:Phylogeny; D013045:Species Specificity; D014774:Virulence / Q000235:genetics*; D015007:Yersinia / Q000235:genetics* / Q000378:metabolism / Q000472:pathogenicity*; D015008:Yersinia enterocolitica / Q000235:genetics / Q000378:metabolism / Q000472:pathogenicity
keywords: Enterobacteriaceae; genomics metabolic streamlining; pathoadaptation
references.citation: Microbiol Rev. 1987 Jun;51(2):192-205
references.pmid: 3299028
references.citation: Nat Rev Microbiol. 2006 Nov;4(11):811-25
references.pmid: 17041629
references.citation: Mol Biol Evol. 2013 May;30(5):1224-8
references.pmid: 23408797
references.citation: Nature. 2010 Sep 23;467(7314):426-9
references.pmid: 20864996
references.citation: Int J Syst Evol Microbiol. 2008 Apr;58(Pt 4):779-84
references.pmid: 18398169
references.citation: J Mol Evol. 2002 Jul;55(1):37-51
references.pmid: 12165841
references.citation: Nature. 2001 Oct 25;413(6858):848-52
references.pmid: 11677608
references.citation: Nature. 2001 Oct 4;413(6855):523-7
references.pmid: 11586360
references.citation: N Engl J Med. 2011 Aug 25;365(8):709-17
references.pmid: 21793740
references.citation: Nat Genet. 2010 Dec;42(12):1140-3
references.pmid: 21037571
references.citation: Math Biosci. 2007 Jan;205(1):19-31
references.pmid: 17087977
references.citation: Trends Microbiol. 1999 May;7(5):191-5
references.pmid: 10354593
references.citation: Environ Microbiol. 2011 Dec;13(12):3114-27
references.pmid: 21951486
references.citation: J Bacteriol. 1981 Dec;148(3):877-83
references.pmid: 6273385
references.citation: Adv Exp Med Biol. 2003;529:3-12
references.pmid: 12756719
references.citation: J Clin Microbiol. 2011 Apr;49(4):1251-9
references.pmid: 21325549
references.citation: Berl Munch Tierarztl Wochenschr. 1997 May;110(5):176-7
references.pmid: 9290039
references.citation: Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13826-31
references.pmid: 15358858
references.citation: Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):906-7
references.pmid: 8570657
references.citation: Nat Rev Microbiol. 2003 Oct;1(1):55-64
references.pmid: 15040180
references.citation: Infect Immun. 1988 May;56(5):1242-8
references.pmid: 2833444
references.citation: Infect Immun. 2004 Aug;72(8):4784-90
references.pmid: 15271940
references.citation: Mol Microbiol. 2007 Oct;66(1):189-205
references.pmid: 17784909
references.citation: J Med Microbiol. 1987 Nov;24(3):219-26
references.pmid: 3669055
references.citation: Curr Top Microbiol Immunol. 2002;264(1):89-108
references.pmid: 12014183
references.citation: Genome Res. 2008 May;18(5):821-9
references.pmid: 18349386
references.citation: BMC Genomics. 2010 Nov 23;11:652
references.pmid: 21092259
references.citation: Infect Immun. 2004 Dec;72(12):6780-9
references.pmid: 15557598
references.citation: BMC Genomics. 2011 Mar 31;12:168
references.pmid: 21453472
references.citation: J Appl Bacteriol. 1982 Apr;52(2):151-83
references.pmid: 7050068
references.citation: Infect Immun. 2001 Jul;69(7):4627-38
references.pmid: 11402007
references.citation: Infect Immun. 2012 Dec;80(12):4061-70
references.pmid: 23045475
references.citation: Contrib Microbiol Immunol. 1987;9:14-21
references.pmid: 3665492
references.citation: FEMS Microbiol Lett. 2001 Dec 18;205(2):159-64
references.pmid: 11750796
references.citation: PLoS Genet. 2006 Dec 15;2(12):e206
references.pmid: 17173484
references.citation: Genome Biol. 2010 Jan 04;11(1):R1
references.pmid: 20047673
references.citation: J Clin Microbiol. 2005 Jun;43(6):2674-84
references.pmid: 15956383
references.citation: J Bacteriol. 1996 Dec;178(23):6743-51
references.pmid: 8955291
references.citation: Science. 2009 Oct 9;326(5950):236-7
references.pmid: 19815760
references.citation: Infect Immun. 2003 Jun;71(6):3512-20
references.pmid: 12761136
references.citation: Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17837-42
references.pmid: 15598742
references.citation: PLoS Genet. 2005 Dec;1(6):e80
references.pmid: 16429164
references.citation: Bioinformatics. 2010 Jul 15;26(14):1704-7
references.pmid: 20562415
references.citation: Adv Exp Med Biol. 2003;529:43-6
references.pmid: 12756726
references.citation: Science. 2010 Jan 22;327(5964):469-74
references.pmid: 20093474
references.citation: J Bacteriol. 2001 Apr;183(8):2463-75
references.pmid: 11274105
references.citation: BMC Genomics. 2011 Jul 06;12:348
references.pmid: 21733159
references.citation: J Bacteriol. 1984 Jul;159(1):206-13
references.pmid: 6376471