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<titleStmt>
<title xml:lang="en">Parallel independent evolution of pathogenicity within the genus
<italic>Yersinia</italic>
</title>
<author>
<name sortKey="Reuter, Sandra" sort="Reuter, Sandra" uniqKey="Reuter S" first="Sandra" last="Reuter">Sandra Reuter</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Connor, Thomas R" sort="Connor, Thomas R" uniqKey="Connor T" first="Thomas R." last="Connor">Thomas R. Connor</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff3">Cardiff University School of Biosciences,
<institution>Cardiff University</institution>
, Cardiff CF10 3AX, Wales,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Barquist, Lars" sort="Barquist, Lars" uniqKey="Barquist L" first="Lars" last="Barquist">Lars Barquist</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Walker, Danielle" sort="Walker, Danielle" uniqKey="Walker D" first="Danielle" last="Walker">Danielle Walker</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Feltwell, Theresa" sort="Feltwell, Theresa" uniqKey="Feltwell T" first="Theresa" last="Feltwell">Theresa Feltwell</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Harris, Simon R" sort="Harris, Simon R" uniqKey="Harris S" first="Simon R." last="Harris">Simon R. Harris</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fookes, Maria" sort="Fookes, Maria" uniqKey="Fookes M" first="Maria" last="Fookes">Maria Fookes</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hall, Miquette E" sort="Hall, Miquette E" uniqKey="Hall M" first="Miquette E." last="Hall">Miquette E. Hall</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Petty, Nicola K" sort="Petty, Nicola K" uniqKey="Petty N" first="Nicola K." last="Petty">Nicola K. Petty</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff4">The ithree institute,
<institution>University of Technology</institution>
, Sydney, NSW 2007,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fuchs, Thilo M" sort="Fuchs, Thilo M" uniqKey="Fuchs T" first="Thilo M." last="Fuchs">Thilo M. Fuchs</name>
<affiliation>
<nlm:aff id="aff5">Zentralinstitut für Ernährungs- und Lebensmittelforschung,
<institution>Technische Universität München</institution>
, D-85350 Freising,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Corander, Jukka" sort="Corander, Jukka" uniqKey="Corander J" first="Jukka" last="Corander">Jukka Corander</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Dufour, Muriel" sort="Dufour, Muriel" uniqKey="Dufour M" first="Muriel" last="Dufour">Muriel Dufour</name>
<affiliation>
<nlm:aff id="aff7">
<institution>Institute of Environmental Science and Research</institution>
, Wallaceville, Upper Hutt 5140,
<country>New Zealand</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ringwood, Tamara" sort="Ringwood, Tamara" uniqKey="Ringwood T" first="Tamara" last="Ringwood">Tamara Ringwood</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff8">Department of Microbiology</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Savin, Cyril" sort="Savin, Cyril" uniqKey="Savin C" first="Cyril" last="Savin">Cyril Savin</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name>
<affiliation>
<nlm:aff id="aff11">Genomics Platform,
<institution>Institut Pasteur</institution>
, 75724 Paris,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Martin, Liliane" sort="Martin, Liliane" uniqKey="Martin L" first="Liliane" last="Martin">Liliane Martin</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Miettinen, Minna" sort="Miettinen, Minna" uniqKey="Miettinen M" first="Minna" last="Miettinen">Minna Miettinen</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shubin, Mikhail" sort="Shubin, Mikhail" uniqKey="Shubin M" first="Mikhail" last="Shubin">Mikhail Shubin</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Riehm, Julia M" sort="Riehm, Julia M" uniqKey="Riehm J" first="Julia M." last="Riehm">Julia M. Riehm</name>
<affiliation>
<nlm:aff id="aff12">Department of Bacteriology, Bundeswehr Institute of Microbiology, D-80937 Munich,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Laukkanen Ninios, Riikka" sort="Laukkanen Ninios, Riikka" uniqKey="Laukkanen Ninios R" first="Riikka" last="Laukkanen-Ninios">Riikka Laukkanen-Ninios</name>
<affiliation>
<nlm:aff id="aff13">Department of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine,
<institution>University of Helsinki</institution>
, FIN-00014 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Sihvonen, Leila M" sort="Sihvonen, Leila M" uniqKey="Sihvonen L" first="Leila M." last="Sihvonen">Leila M. Sihvonen</name>
<affiliation>
<nlm:aff id="aff14">Bacteriology Unit,
<institution>National Institute for Health and Welfare</institution>
(THL), FIN-00271 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Siitonen, Anja" sort="Siitonen, Anja" uniqKey="Siitonen A" first="Anja" last="Siitonen">Anja Siitonen</name>
<affiliation>
<nlm:aff id="aff14">Bacteriology Unit,
<institution>National Institute for Health and Welfare</institution>
(THL), FIN-00271 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Skurnik, Mikael" sort="Skurnik, Mikael" uniqKey="Skurnik M" first="Mikael" last="Skurnik">Mikael Skurnik</name>
<affiliation>
<nlm:aff id="aff15">Department of Bacteriology and Immunology, Haartman Institute,
<institution>University of Helsinki</institution>
and Helsinki University Central Hospital Laboratory Diagnostics, FIN-00014 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Falcao, Juliana Pfrimer" sort="Falcao, Juliana Pfrimer" uniqKey="Falcao J" first="Juliana Pfrimer" last="Falcão">Juliana Pfrimer Falcão</name>
<affiliation>
<nlm:aff id="aff16">Brazilian Reference Center on
<italic>Yersinia</italic>
spp. other than
<italic>Y. pestis</italic>
, Faculdade de Ciências Farmacêuticas de Ribeirão Preto–
<institution>Universidade São Paulo</institution>
, Ribeirão Preto, CEP 14040-903, São Paulo,
<country>Brazil</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fukushima, Hiroshi" sort="Fukushima, Hiroshi" uniqKey="Fukushima H" first="Hiroshi" last="Fukushima">Hiroshi Fukushima</name>
<affiliation>
<nlm:aff id="aff17">
<institution>Shimane Prefectural Institute of Public Health and Environmental Science</institution>
, Matsue, Shimane 699-0122,
<country>Japan</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Scholz, Holger C" sort="Scholz, Holger C" uniqKey="Scholz H" first="Holger C." last="Scholz">Holger C. Scholz</name>
<affiliation>
<nlm:aff id="aff12">Department of Bacteriology, Bundeswehr Institute of Microbiology, D-80937 Munich,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Prentice, Michael B" sort="Prentice, Michael B" uniqKey="Prentice M" first="Michael B." last="Prentice">Michael B. Prentice</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff8">Department of Microbiology</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wren, Brendan W" sort="Wren, Brendan W" uniqKey="Wren B" first="Brendan W." last="Wren">Brendan W. Wren</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff18">Department of Infectious and Tropical Diseases,
<institution>London School of Hygiene and Tropical Medicine</institution>
, London WC1E 7HT,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Parkhill, Julian" sort="Parkhill, Julian" uniqKey="Parkhill J" first="Julian" last="Parkhill">Julian Parkhill</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Carniel, Elisabeth" sort="Carniel, Elisabeth" uniqKey="Carniel E" first="Elisabeth" last="Carniel">Elisabeth Carniel</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Achtman, Mark" sort="Achtman, Mark" uniqKey="Achtman M" first="Mark" last="Achtman">Mark Achtman</name>
<affiliation>
<nlm:aff id="aff9">Environmental Research Institute,
<institution>University College Cork</institution>
, Cork,
<country>Ireland</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff19">Warwick Medical School,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mcnally, Alan" sort="Mcnally, Alan" uniqKey="Mcnally A" first="Alan" last="Mcnally">Alan Mcnally</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Thomson, Nicholas R" sort="Thomson, Nicholas R" uniqKey="Thomson N" first="Nicholas R." last="Thomson">Nicholas R. Thomson</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff18">Department of Infectious and Tropical Diseases,
<institution>London School of Hygiene and Tropical Medicine</institution>
, London WC1E 7HT,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt>
<idno type="wicri:source">PMC</idno>
<idno type="pmid">24753568</idno>
<idno type="pmc">4020045</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4020045</idno>
<idno type="RBID">PMC:4020045</idno>
<idno type="doi">10.1073/pnas.1317161111</idno>
<date when="2014">2014</date>
<idno type="wicri:Area/Pmc/Corpus">001B94</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001B94</idno>
</publicationStmt>
<sourceDesc>
<biblStruct>
<analytic>
<title xml:lang="en" level="a" type="main">Parallel independent evolution of pathogenicity within the genus
<italic>Yersinia</italic>
</title>
<author>
<name sortKey="Reuter, Sandra" sort="Reuter, Sandra" uniqKey="Reuter S" first="Sandra" last="Reuter">Sandra Reuter</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Connor, Thomas R" sort="Connor, Thomas R" uniqKey="Connor T" first="Thomas R." last="Connor">Thomas R. Connor</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff3">Cardiff University School of Biosciences,
<institution>Cardiff University</institution>
, Cardiff CF10 3AX, Wales,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Barquist, Lars" sort="Barquist, Lars" uniqKey="Barquist L" first="Lars" last="Barquist">Lars Barquist</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Walker, Danielle" sort="Walker, Danielle" uniqKey="Walker D" first="Danielle" last="Walker">Danielle Walker</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Feltwell, Theresa" sort="Feltwell, Theresa" uniqKey="Feltwell T" first="Theresa" last="Feltwell">Theresa Feltwell</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Harris, Simon R" sort="Harris, Simon R" uniqKey="Harris S" first="Simon R." last="Harris">Simon R. Harris</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fookes, Maria" sort="Fookes, Maria" uniqKey="Fookes M" first="Maria" last="Fookes">Maria Fookes</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hall, Miquette E" sort="Hall, Miquette E" uniqKey="Hall M" first="Miquette E." last="Hall">Miquette E. Hall</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Petty, Nicola K" sort="Petty, Nicola K" uniqKey="Petty N" first="Nicola K." last="Petty">Nicola K. Petty</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff4">The ithree institute,
<institution>University of Technology</institution>
, Sydney, NSW 2007,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fuchs, Thilo M" sort="Fuchs, Thilo M" uniqKey="Fuchs T" first="Thilo M." last="Fuchs">Thilo M. Fuchs</name>
<affiliation>
<nlm:aff id="aff5">Zentralinstitut für Ernährungs- und Lebensmittelforschung,
<institution>Technische Universität München</institution>
, D-85350 Freising,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Corander, Jukka" sort="Corander, Jukka" uniqKey="Corander J" first="Jukka" last="Corander">Jukka Corander</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Dufour, Muriel" sort="Dufour, Muriel" uniqKey="Dufour M" first="Muriel" last="Dufour">Muriel Dufour</name>
<affiliation>
<nlm:aff id="aff7">
<institution>Institute of Environmental Science and Research</institution>
, Wallaceville, Upper Hutt 5140,
<country>New Zealand</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ringwood, Tamara" sort="Ringwood, Tamara" uniqKey="Ringwood T" first="Tamara" last="Ringwood">Tamara Ringwood</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff8">Department of Microbiology</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Savin, Cyril" sort="Savin, Cyril" uniqKey="Savin C" first="Cyril" last="Savin">Cyril Savin</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name>
<affiliation>
<nlm:aff id="aff11">Genomics Platform,
<institution>Institut Pasteur</institution>
, 75724 Paris,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Martin, Liliane" sort="Martin, Liliane" uniqKey="Martin L" first="Liliane" last="Martin">Liliane Martin</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Miettinen, Minna" sort="Miettinen, Minna" uniqKey="Miettinen M" first="Minna" last="Miettinen">Minna Miettinen</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shubin, Mikhail" sort="Shubin, Mikhail" uniqKey="Shubin M" first="Mikhail" last="Shubin">Mikhail Shubin</name>
<affiliation>
<nlm:aff wicri:cut=", and" id="aff6">Department of Mathematics and Statistics</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Riehm, Julia M" sort="Riehm, Julia M" uniqKey="Riehm J" first="Julia M." last="Riehm">Julia M. Riehm</name>
<affiliation>
<nlm:aff id="aff12">Department of Bacteriology, Bundeswehr Institute of Microbiology, D-80937 Munich,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Laukkanen Ninios, Riikka" sort="Laukkanen Ninios, Riikka" uniqKey="Laukkanen Ninios R" first="Riikka" last="Laukkanen-Ninios">Riikka Laukkanen-Ninios</name>
<affiliation>
<nlm:aff id="aff13">Department of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine,
<institution>University of Helsinki</institution>
, FIN-00014 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Sihvonen, Leila M" sort="Sihvonen, Leila M" uniqKey="Sihvonen L" first="Leila M." last="Sihvonen">Leila M. Sihvonen</name>
<affiliation>
<nlm:aff id="aff14">Bacteriology Unit,
<institution>National Institute for Health and Welfare</institution>
(THL), FIN-00271 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Siitonen, Anja" sort="Siitonen, Anja" uniqKey="Siitonen A" first="Anja" last="Siitonen">Anja Siitonen</name>
<affiliation>
<nlm:aff id="aff14">Bacteriology Unit,
<institution>National Institute for Health and Welfare</institution>
(THL), FIN-00271 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Skurnik, Mikael" sort="Skurnik, Mikael" uniqKey="Skurnik M" first="Mikael" last="Skurnik">Mikael Skurnik</name>
<affiliation>
<nlm:aff id="aff15">Department of Bacteriology and Immunology, Haartman Institute,
<institution>University of Helsinki</institution>
and Helsinki University Central Hospital Laboratory Diagnostics, FIN-00014 Helsinki,
<country>Finland</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Falcao, Juliana Pfrimer" sort="Falcao, Juliana Pfrimer" uniqKey="Falcao J" first="Juliana Pfrimer" last="Falcão">Juliana Pfrimer Falcão</name>
<affiliation>
<nlm:aff id="aff16">Brazilian Reference Center on
<italic>Yersinia</italic>
spp. other than
<italic>Y. pestis</italic>
, Faculdade de Ciências Farmacêuticas de Ribeirão Preto–
<institution>Universidade São Paulo</institution>
, Ribeirão Preto, CEP 14040-903, São Paulo,
<country>Brazil</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Fukushima, Hiroshi" sort="Fukushima, Hiroshi" uniqKey="Fukushima H" first="Hiroshi" last="Fukushima">Hiroshi Fukushima</name>
<affiliation>
<nlm:aff id="aff17">
<institution>Shimane Prefectural Institute of Public Health and Environmental Science</institution>
, Matsue, Shimane 699-0122,
<country>Japan</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Scholz, Holger C" sort="Scholz, Holger C" uniqKey="Scholz H" first="Holger C." last="Scholz">Holger C. Scholz</name>
<affiliation>
<nlm:aff id="aff12">Department of Bacteriology, Bundeswehr Institute of Microbiology, D-80937 Munich,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Prentice, Michael B" sort="Prentice, Michael B" uniqKey="Prentice M" first="Michael B." last="Prentice">Michael B. Prentice</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff8">Department of Microbiology</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wren, Brendan W" sort="Wren, Brendan W" uniqKey="Wren B" first="Brendan W." last="Wren">Brendan W. Wren</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff18">Department of Infectious and Tropical Diseases,
<institution>London School of Hygiene and Tropical Medicine</institution>
, London WC1E 7HT,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Parkhill, Julian" sort="Parkhill, Julian" uniqKey="Parkhill J" first="Julian" last="Parkhill">Julian Parkhill</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Carniel, Elisabeth" sort="Carniel, Elisabeth" uniqKey="Carniel E" first="Elisabeth" last="Carniel">Elisabeth Carniel</name>
<affiliation>
<nlm:aff id="aff10">
<italic>Yersinia</italic>
Research Unit,</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Achtman, Mark" sort="Achtman, Mark" uniqKey="Achtman M" first="Mark" last="Achtman">Mark Achtman</name>
<affiliation>
<nlm:aff id="aff9">Environmental Research Institute,
<institution>University College Cork</institution>
, Cork,
<country>Ireland</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff19">Warwick Medical School,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mcnally, Alan" sort="Mcnally, Alan" uniqKey="Mcnally A" first="Alan" last="Mcnally">Alan Mcnally</name>
<affiliation>
<nlm:aff id="aff1">Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Thomson, Nicholas R" sort="Thomson, Nicholas R" uniqKey="Thomson N" first="Nicholas R." last="Thomson">Nicholas R. Thomson</name>
<affiliation>
<nlm:aff id="aff2">Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff18">Department of Infectious and Tropical Diseases,
<institution>London School of Hygiene and Tropical Medicine</institution>
, London WC1E 7HT,
<country>United Kingdom</country>
</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
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<front>
<div type="abstract" xml:lang="en">
<title>Significance</title>
<p>Our past understanding of pathogen evolution has been fragmented because of tendencies to study human clinical isolates. To understand the evolutionary trends of pathogenic bacteria though, we need the context of their nonpathogenic relatives. Our unique and detailed dataset allows description of the parallel evolution of two key human pathogens: the causative agents of plague and
<italic>Yersinia</italic>
diarrhea. The analysis reveals an emerging pattern where few virulence-related functions are found in all pathogenic lineages, representing key “foothold” moments that mark the emergence of these pathogens. Functional gene loss and metabolic streamlining are equally complementing the evolution of
<italic>Yersinia</italic>
across the pathogenic spectrum.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group>
<journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher>
<publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24753568</article-id>
<article-id pub-id-type="pmc">4020045</article-id>
<article-id pub-id-type="publisher-id">201317161</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1317161111</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Microbiology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Parallel independent evolution of pathogenicity within the genus
<italic>Yersinia</italic>
</article-title>
<alt-title alt-title-type="short">Independent evolution of
<italic>Yersinia</italic>
pathogenicity</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Reuter</surname>
<given-names>Sandra</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Connor</surname>
<given-names>Thomas R.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Barquist</surname>
<given-names>Lars</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Walker</surname>
<given-names>Danielle</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Feltwell</surname>
<given-names>Theresa</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Harris</surname>
<given-names>Simon R.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fookes</surname>
<given-names>Maria</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hall</surname>
<given-names>Miquette E.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Petty</surname>
<given-names>Nicola K.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fuchs</surname>
<given-names>Thilo M.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Corander</surname>
<given-names>Jukka</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dufour</surname>
<given-names>Muriel</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ringwood</surname>
<given-names>Tamara</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Savin</surname>
<given-names>Cyril</given-names>
</name>
<xref ref-type="aff" rid="aff10">
<sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bouchier</surname>
<given-names>Christiane</given-names>
</name>
<xref ref-type="aff" rid="aff11">
<sup>j</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Martin</surname>
<given-names>Liliane</given-names>
</name>
<xref ref-type="aff" rid="aff10">
<sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Miettinen</surname>
<given-names>Minna</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shubin</surname>
<given-names>Mikhail</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Riehm</surname>
<given-names>Julia M.</given-names>
</name>
<xref ref-type="aff" rid="aff12">
<sup>k</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Laukkanen-Ninios</surname>
<given-names>Riikka</given-names>
</name>
<xref ref-type="aff" rid="aff13">
<sup>l</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sihvonen</surname>
<given-names>Leila M.</given-names>
</name>
<xref ref-type="aff" rid="aff14">
<sup>m</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Siitonen</surname>
<given-names>Anja</given-names>
</name>
<xref ref-type="aff" rid="aff14">
<sup>m</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Skurnik</surname>
<given-names>Mikael</given-names>
</name>
<xref ref-type="aff" rid="aff15">
<sup>n</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Falcão</surname>
<given-names>Juliana Pfrimer</given-names>
</name>
<xref ref-type="aff" rid="aff16">
<sup>o</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fukushima</surname>
<given-names>Hiroshi</given-names>
</name>
<xref ref-type="aff" rid="aff17">
<sup>p</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Scholz</surname>
<given-names>Holger C.</given-names>
</name>
<xref ref-type="aff" rid="aff12">
<sup>k</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Prentice</surname>
<given-names>Michael B.</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wren</surname>
<given-names>Brendan W.</given-names>
</name>
<xref ref-type="aff" rid="aff18">
<sup>q</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Parkhill</surname>
<given-names>Julian</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Carniel</surname>
<given-names>Elisabeth</given-names>
</name>
<xref ref-type="aff" rid="aff10">
<sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Achtman</surname>
<given-names>Mark</given-names>
</name>
<xref ref-type="aff" rid="aff9">
<sup>r</sup>
</xref>
<xref ref-type="aff" rid="aff19">
<sup>s</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>McNally</surname>
<given-names>Alan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Thomson</surname>
<given-names>Nicholas R.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff18">
<sup>q</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>2</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
Pathogen Research Group,
<institution>Nottingham Trent University</institution>
, Nottingham NG11 8NS,
<country>United Kingdom</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
Pathogen Genomics,
<institution>Wellcome Trust Sanger Institute</institution>
, Cambridge CB10 1SA,
<country>United Kingdom</country>
;</aff>
<aff id="aff3">
<sup>c</sup>
Cardiff University School of Biosciences,
<institution>Cardiff University</institution>
, Cardiff CF10 3AX, Wales,
<country>United Kingdom</country>
;</aff>
<aff id="aff4">
<sup>d</sup>
The ithree institute,
<institution>University of Technology</institution>
, Sydney, NSW 2007,
<country>Australia</country>
;</aff>
<aff id="aff5">
<sup>e</sup>
Zentralinstitut für Ernährungs- und Lebensmittelforschung,
<institution>Technische Universität München</institution>
, D-85350 Freising,
<country>Germany</country>
;</aff>
<aff id="aff6">
<sup>f</sup>
Department of Mathematics and Statistics, and</aff>
<aff id="aff13">
<sup>l</sup>
Department of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine,
<institution>University of Helsinki</institution>
, FIN-00014 Helsinki,
<country>Finland</country>
;</aff>
<aff id="aff7">
<sup>g</sup>
<institution>Institute of Environmental Science and Research</institution>
, Wallaceville, Upper Hutt 5140,
<country>New Zealand</country>
;</aff>
<aff id="aff8">
<sup>h</sup>
Department of Microbiology and</aff>
<aff id="aff9">
<sup>r</sup>
Environmental Research Institute,
<institution>University College Cork</institution>
, Cork,
<country>Ireland</country>
;</aff>
<aff id="aff10">
<sup>i</sup>
<italic>Yersinia</italic>
Research Unit,</aff>
<aff id="aff11">
<sup>j</sup>
Genomics Platform,
<institution>Institut Pasteur</institution>
, 75724 Paris,
<country>France</country>
;</aff>
<aff id="aff12">
<sup>k</sup>
Department of Bacteriology, Bundeswehr Institute of Microbiology, D-80937 Munich,
<country>Germany</country>
;</aff>
<aff id="aff14">
<sup>m</sup>
Bacteriology Unit,
<institution>National Institute for Health and Welfare</institution>
(THL), FIN-00271 Helsinki,
<country>Finland</country>
;</aff>
<aff id="aff15">
<sup>n</sup>
Department of Bacteriology and Immunology, Haartman Institute,
<institution>University of Helsinki</institution>
and Helsinki University Central Hospital Laboratory Diagnostics, FIN-00014 Helsinki,
<country>Finland</country>
;</aff>
<aff id="aff16">
<sup>o</sup>
Brazilian Reference Center on
<italic>Yersinia</italic>
spp. other than
<italic>Y. pestis</italic>
, Faculdade de Ciências Farmacêuticas de Ribeirão Preto–
<institution>Universidade São Paulo</institution>
, Ribeirão Preto, CEP 14040-903, São Paulo,
<country>Brazil</country>
;</aff>
<aff id="aff17">
<sup>p</sup>
<institution>Shimane Prefectural Institute of Public Health and Environmental Science</institution>
, Matsue, Shimane 699-0122,
<country>Japan</country>
;</aff>
<aff id="aff18">
<sup>q</sup>
Department of Infectious and Tropical Diseases,
<institution>London School of Hygiene and Tropical Medicine</institution>
, London WC1E 7HT,
<country>United Kingdom</country>
; and</aff>
<aff id="aff19">
<sup>s</sup>
Warwick Medical School,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>2</sup>
To whom correspondence should be addressed. E-mail:
<email>nrt@sanger.ac.uk</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Ralph R. Isberg, Howard Hughes Medical Institute and Tufts University School of Medicine, Boston, MA, and approved March 21, 2014 (received for review October 2, 2013)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: S.R., T.R.C., B.W.W., J.P., M.A., A.M., and N.R.T. designed research; S.R., T.R.C., L.B., D.W., T.F., S.R.H., M.F., M.E.H., N.K.P., J.C., M.M., M. Shubin, and N.R.T. performed research; T.M.F., M.D., T.R., C.S., C.B., L.M., J.M.R., R.L.-N., L.M.S., A.S., J.P.F., H.F., and H.C.S. were involved in isolate collection and typing; S.R., T.R.C., L.B., D.W., S.R.H., M.F., M.E.H., N.K.P., J.C., M.M., M. Shubin, and N.R.T. analyzed data; and S.R., T.R.C., L.B., S.R.H., T.M.F., M. Skurnik, M.B.P., B.W.W., J.P., E.C., M.A., A.M., and N.R.T. wrote the paper.</p>
</fn>
<fn fn-type="equal" id="fn1">
<p>
<sup>1</sup>
S.R. and T.R.C. contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>6</day>
<month>5</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>21</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>21</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>111</volume>
<issue>18</issue>
<fpage>6768</fpage>
<lpage>6773</lpage>
<permissions>
<license license-type="open-access">
<license-p>Freely available online through the PNAS open access option.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201317161.pdf"></self-uri>
<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>Our past understanding of pathogen evolution has been fragmented because of tendencies to study human clinical isolates. To understand the evolutionary trends of pathogenic bacteria though, we need the context of their nonpathogenic relatives. Our unique and detailed dataset allows description of the parallel evolution of two key human pathogens: the causative agents of plague and
<italic>Yersinia</italic>
diarrhea. The analysis reveals an emerging pattern where few virulence-related functions are found in all pathogenic lineages, representing key “foothold” moments that mark the emergence of these pathogens. Functional gene loss and metabolic streamlining are equally complementing the evolution of
<italic>Yersinia</italic>
across the pathogenic spectrum.</p>
</abstract>
<abstract>
<p>The genus
<italic>Yersinia</italic>
has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all
<italic>Yersinia</italic>
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
<italic>Yersinia</italic>
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
<italic>ail</italic>
. 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.</p>
</abstract>
<kwd-group>
<kwd>genomics metabolic streamlining</kwd>
<kwd>pathoadaptation</kwd>
<kwd>
<italic>Enterobacteriaceae</italic>
</kwd>
</kwd-group>
<counts>
<page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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