{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,16]],"date-time":"2026-05-16T03:35:54Z","timestamp":1778902554010,"version":"3.51.4"},"reference-count":40,"publisher":"Proceedings of the National Academy of Sciences","issue":"51","content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2004,12,21]]},"abstract":"<jats:p>\n                    The association of historical plague pandemics with\n                    <jats:italic>Yersinia pestis<\/jats:italic>\n                    remains controversial, partly because the evolutionary history of this largely monomorphic bacterium was unknown. The microevolution of\n                    <jats:italic>Y. pestis<\/jats:italic>\n                    was therefore investigated by three different multilocus molecular methods, targeting genomewide synonymous SNPs, variation in number of tandem repeats, and insertion of IS\n                    <jats:italic>100<\/jats:italic>\n                    insertion elements. Eight populations were recognized by the three methods, and we propose an evolutionary tree for these populations, rooted on\n                    <jats:italic>Yersinia pseudotuberculosis<\/jats:italic>\n                    . The tree invokes microevolution over millennia, during which enzootic pestoides isolates evolved. This initial phase was followed by a binary split 6,500 years ago, which led to populations that are more frequently associated with human disease. These populations do not correspond directly to classical biovars that are based on phenotypic properties. Thus, we recommend that henceforth groupings should be based on molecular signatures. The age of\n                    <jats:italic>Y. pestis<\/jats:italic>\n                    inferred here is compatible with the dates of historical pandemic plague. However, it is premature to infer an association between any modern molecular grouping and a particular pandemic wave that occurred before the 20th century.\n                  <\/jats:p>","DOI":"10.1073\/pnas.0408026101","type":"journal-article","created":{"date-parts":[[2004,12,14]],"date-time":"2004-12-14T21:58:07Z","timestamp":1103061487000},"page":"17837-17842","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":419,"title":["Microevolution and history of the plague bacillus,\n                    <i>Yersinia pestis<\/i>"],"prefix":"10.1073","volume":"101","author":[{"given":"Mark","family":"Achtman","sequence":"first","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giovanna","family":"Morelli","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peixuan","family":"Zhu","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thierry","family":"Wirth","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ines","family":"Diehl","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Barica","family":"Kusecek","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amy J.","family":"Vogler","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David M.","family":"Wagner","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christopher J.","family":"Allender","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"W. Ryan","family":"Easterday","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Viviane","family":"Chenal-Francisque","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patricia","family":"Worsham","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicholas R.","family":"Thomson","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julian","family":"Parkhill","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luther E.","family":"Lindler","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; National Biodefense Analysis and Countermeasures Center,..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elisabeth","family":"Carniel","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Max-Planck Institut f\u00fcr Infektionsbiologie, D-10117 Berlin, Germany; Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640; Yersinia Research Unit, Institut Pasteur, 75724 Paris Cedex 15, France; U.S. Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD 21702-5011; The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; 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