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Nat Microbiol. 2016 Mar 21;1:16027. doi: 10.1038/nmicrobiol.2016.27.

Global phylogeography and evolutionary history of Shigella dysenteriae type 1.

Author information

1
Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France.
2
Centre for Systems Genomics, University of Melbourne, Parkville, Victoria 3010, Australia.
3
Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia.
4
School of Agriculture and Veterinary Science, University of Melbourne, Parkville, Victoria 3010, Australia.
5
Centers for Disease Control and Prevention, Escherichia and Shigella Reference Unit, Atlanta, Georgia 30333, USA.
6
Public Health England, Gastrointestinal Bacteria Reference Unit, Colindale NW9 5HT, UK.
7
icddr,b, Enteric and Food Microbiology Laboratory, Dhaka 1212, Bangladesh.
8
Institut Pasteur de Bangui, BP 923, Bangui, République Centrafricaine.
9
Institut Pasteur de Dakar, BP 220, Dakar, Senegal.
10
Federal Budget Institute of Science, Central Research Institute for Epidemiology, Moscow 111123, Russia.
11
Czech National Collection of Type Cultures (CNCTC), National Institute of Public Health, Prague 10, Czech Republic.
12
Public Health England, National Collection of Type Cultures, Porton Down SP4 0JG, UK.
13
Pasteur Institute of St Petersburg, St Petersburg 197101, Russia.
14
Department of Medical Microbiology, University of KwaZulu-Natal, Durban 4041, South Africa.
15
Department of Microbiology, LHUB-ULB, Brussels University Hospitals Laboratory, 1000 Brussels, Belgium.
16
Environmental Health Research Centre, Public Health School, Université Libre de Bruxelles, 1070 Brussels, Belgium.
17
Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK.
18
Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK.
19
Armed Forces Research Institute of Medical Sciences (AFRIMS), Bangkok 10400, Thailand.
20
National Institute of Cholera and Enteric Diseases (NICED), Kolkata, West Bengal 700010, India.
21
Institut Pasteur, Collection de l'Institut Pasteur (CIP), 75724 Paris Cedex 15, France.
22
Polish Collection of Microorganisms, Institute of Immunology and Experimental Therapy, 53-114 Wroclaw, Poland.
23
Institut Pasteur, Plate-forme Génomique (PF1), 75724 Paris Cedex 15, France.
24
Department of Foodborne Infections, Norwegian Institute of Public Health, Nydalen 0403, Oslo, Norway.
25
Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroon.
26
Departments of Medicine and Microbiology, New York University Langone Medical Center, New York, New York 10016, USA.
27
Public Health Agency of Sweden, 17182 Solna, Sweden.
28
Biology Department and Infection Control Unit, Bégin Military Hospital, 94160 Saint-Mandé, France.
29
Epicentre, 75011 Paris, France.
30
Institut für Hygiene und Umwelt, 20539 Hamburg, Germany.
31
Divison of Enteropathogenic Bacteria and Legionella, Robert Koch Institut, 38855 Wernigerode, Germany.
32
INSERM, IAME, UMR 1137, Univ. Paris Diderot, IAME, UMR 1137, Sorbonne Paris Cité, 75018 Paris, France.
33
Bacterial Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland 20910, USA.
34
Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem 91120, Israel.
35
Center of Research and Diagnostics, Centers for Disease Control, Taichung 40855, Taiwan.
36
Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Biologia e Biotecnologie C Darwin, Sapienza Università di Roma, 00185, Roma, Italy.
37
Central Laboratories, Ministry of Health, Jerusalem 91342, Israel.
38
Institut Pasteur, Genotyping of Pathogens and Public Health Platform, 75724 Paris Cedex 15, France.
39
Department of Bacteriology I, National Institute of Infectious Diseases, Tokyo, 162-8640, Japan.
40
Department of Sera and Vaccines Evaluation, National Institute of Public Health-National Institute of Hygiene, 00-791 Warsaw, Poland.
41
National Reference Laboratory for E. coli and Shigella, National Institute of Public Health, Prague 10, Czech Republic.
42
National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba R3E 3R2, Canada.
43
Institut Pasteur, Bioinformatics platform, 75724 Paris Cedex 15, France.
44
State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China.
45
Department of Clinical Microbiology, Faculty of Medicine and University Hospital, Charles University, 500 05, Hradec Kralove, Czech Republic.
46
Hungarian National Collection of Medical Bacteria, National Center for Epidemiology, H-1097 Budapest, Hungary.
47
Institut Pasteur, Unité de Pathogénie Microbienne Moléculaire, 75724 Paris Cedex 15, France.
48
Institut Pasteur, Microbial Evolutionary Genomics Unit, 75724 Paris Cedex 15, France.
49
CNRS, UMR 3525, 75015 Paris, France.
50
London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK.

Abstract

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.

PMID:
27572446
DOI:
10.1038/nmicrobiol.2016.27
[Indexed for MEDLINE]

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