Together with plague, smallpox and typhus, epidemics of dysentery have been a major scourge of human populations for centuries(1). A previous genomic study concluded that Shigella dysenteriae type 1 (Sd1), the epidemic dysentery bacillus, emerged and spread worldwide after the First World War, with no clear pattern of transmission(2). This is not consistent with the massive cyclic dysentery epidemics reported in Europe during the eighteenth and nineteenth centuries(1,3,4) and the first isolation of Sd1 in Japan in 1897(5). Here, we report a whole-genome analysis of 331 Sd1 isolates from around the world, collected between 1915 and 2011, providing us with unprecedented insight into the historical spread of this pathogen. We show here that Sd1 has existed since at least the eighteenth century and that it swept the globe at the end of the nineteenth century, diversifying into distinct lineages associated with the First World War, Second World War and various conflicts or natural disasters across Africa, Asia and Central America. We also provide a unique historical perspective on the evolution of antibiotic resistance over a 100-year period, beginning decades before the antibiotic era, and identify a prevalent multiple antibiotic-resistant lineage in South Asia that was transmitted in several waves to Africa, where it caused severe outbreaks of disease.

Armed Forces Research Institute of Medical Sciences Bangkok 10400 Thailand

Bacterial Diseases Branch Walter Reed Army Institute of Research Silver Spring Maryland 20910 USA

Biology Department and Infection Control Unit Bégin Military Hospital 94160 Saint Mandé France

Center of Research and Diagnostics Centers for Disease Control Taichung 40855 Taiwan

Centers for Disease Control and Prevention Escherichia and Shigella Reference Unit Atlanta Georgia 30333 USA

Central Laboratories Ministry of Health Jerusalem 91342 Israel

Centre for Systems Genomics University of Melbourne Parkville Victoria 3010 Australia

Centre Pasteur du Cameroun BP 1274 Yaoundé Cameroon

CNRS UMR 3525 75015 Paris France

Czech National Collection of Type Cultures National Institute of Public Health Prague 10 Czech Republic

Department of Bacteriology 1 National Institute of Infectious Diseases Tokyo 162 8640 Japan

Department of Biochemistry and Molecular Biology Bio21 Molecular Science and Biotechnology Institute University of Melbourne Parkville Victoria 3010 Australia

Department of Clinical Microbiology Faculty of Medicine and University Hospital Charles University 500 05 Hradec Kralove Czech Republic

Department of Foodborne Infections Norwegian Institute of Public Health Nydalen 0403 Oslo Norway

Department of Medical Microbiology University of KwaZulu Natal Durban 4041 South Africa

Department of Microbiology LHUB ULB Brussels University Hospitals Laboratory 1000 Brussels Belgium

Department of Sera and Vaccines Evaluation National Institute of Public Health National Institute of Hygiene 00 791 Warsaw Poland

Department of Veterinary Medicine University of Cambridge Cambridge CB3 0ES UK

Departments of Medicine and Microbiology New York University Langone Medical Center New York New York 10016 USA

Divison of Enteropathogenic Bacteria and Legionella Robert Koch Institut 38855 Wernigerode Germany

Environmental Health Research Centre Public Health School Université Libre de Bruxelles 1070 Brussels Belgium

Epicentre 75011 Paris France

Faculty of Medicine Hebrew University of Jerusalem Jerusalem 91120 Israel

Federal Budget Institute of Science Central Research Institute for Epidemiology Moscow 111123 Russia

Hungarian National Collection of Medical Bacteria National Center for Epidemiology H 1097 Budapest Hungary

icddr b Enteric and Food Microbiology Laboratory Dhaka 1212 Bangladesh

INSERM IAME UMR 1137 Univ Paris Diderot IAME UMR 1137 Sorbonne Paris Cité 75018 Paris France

Institut für Hygiene und Umwelt 20539 Hamburg Germany

Institut Pasteur Bioinformatics platform 75724 Paris Cedex 15 France

Institut Pasteur Collection de l'Institut Pasteur 75724 Paris Cedex 15 France

Institut Pasteur de Bangui BP 923 Bangui République Centrafricaine

Institut Pasteur de Dakar BP 220 Dakar Senegal

Institut Pasteur Genotyping of Pathogens and Public Health Platform 75724 Paris Cedex 15 France

Institut Pasteur Microbial Evolutionary Genomics Unit 75724 Paris Cedex 15 France

Institut Pasteur Plate forme Génomique 75724 Paris Cedex 15 France

Institut Pasteur Unité de Pathogénie Microbienne Moléculaire 75724 Paris Cedex 15 France

Institut Pasteur Unité des Bactéries Pathogènes Entériques 75724 Paris Cedex 15 France

Istituto Pasteur Fondazione Cenci Bolognetti Dipartimento di Biologia e Biotecnologie C Darwin Sapienza Università di Roma 00185 Roma Italy

London School of Hygiene and Tropical Medicine London WC1E 7HT UK

National Institute of Cholera and Enteric Diseases Kolkata West Bengal 700010 India

National Microbiology Laboratory Public Health Agency of Canada Winnipeg Manitoba R3E 3R2 Canada

National Reference Laboratory for E coli and Shigella National Institute of Public Health Prague 10 Czech Republic

Pasteur Institute of St Petersburg St Petersburg 197101 Russia

Polish Collection of Microorganisms Institute of Immunology and Experimental Therapy 53 114 Wroclaw Poland

Public Health Agency of Sweden 17182 Solna Sweden

Public Health England Gastrointestinal Bacteria Reference Unit Colindale NW9 5HT UK

Public Health England National Collection of Type Cultures Porton Down SP4 0JG UK

School of Agriculture and Veterinary Science University of Melbourne Parkville Victoria 3010 Australia

State Key Laboratory of Infectious Disease Prevention and Control National Institute for Communicable Disease Control and Prevention China CDC Beijing 102206 China

Wellcome Trust Sanger Institute Cambridge CB10 1SA UK

Erratum v

Nat Microbiol. 2016 Oct 03;1(11):16209. doi: 10.1038/nmicrobiol.2016.209. PubMed

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