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Global phylogeography and evolutionary history of Shigella dysenteriae type 1

Nature Microbiology volume 1, Article number: 16027 (2016) Cite this article

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An Erratum to this article was published on 03 October 2016

Abstract

Together with plague, smallpox and typhus, epidemics of dysentery have been a major scourge of human populations for centuries1. 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 transmission2. This is not consistent with the massive cyclic dysentery epidemics reported in Europe during the eighteenth and nineteenth centuries1,3,4 and the first isolation of Sd1 in Japan in 18975. 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.

January 2016 marks one hundred years since the invasion force from Britain, Australia, New Zealand and France withdrew from the Dardanelles, in the then Ottoman Empire, only eight months after landing. Most of the more than 120,000 casualties evacuated from the Gallipoli Peninsula were suffering from epidemic bacillary dysentery6, caused by Shigella dysenteriae type 17,8 (Sd1), a bacterium producing the powerful Shiga toxin. This human-adapted clone of Escherichia coli9 was isolated for the first time by Kiyoshi Shiga during a dysentery outbreak in Japan, during which 90,000 cases and 20,000 deaths occurred in the last six months of 1897 alone5. In the second half of the twentieth century, large outbreaks of disease due to Sd1 were still being reported in Central America, with estimates of more than 500,000 cases and 20,000 deaths for the 1969–1973 epidemic10,11, in Africa, where there were an estimated 100,000 cases and 5,000–10,000 deaths in the 1979 epidemic12, and in Asia13,14.

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Figure 1: Geographic distribution and transmission patterns of Shigella dysenteriae type 1 genetic lineages.
Figure 2: Timed phylogeny of a subsample of 125 Shigella dysenteriae type 1 isolates.
Figure 3: Phenotypic and genetic characterization of antibiotic resistance in Shigella dysenteriae type 1.
Figure 4: Evolution of antibiotic resistance of Shigella dysenteriae type 1.

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Acknowledgements

This study was supported by the Institut Pasteur and the Institut Pasteur International Network, the Institut de Veille Sanitaire, the French government's Investissement d'Avenir programme, Laboratoire d'Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID), the Fondation ‘Le Roch-Les Mousquetaires’, the Canetti family through the Georges, Jacques et Elias Canetti Award 2013, the Wellcome Trust through grant 098051 to the Sanger Institute, the NHMRC of Australia (grant 1061409 to K.E.H), the Victorian Life Sciences Computation Initiative (VLSCI) (grant VR0082) and the Indian Council of Medical Research, New Delhi, India. The authors thank A. Dautry-Versat, A.P. Pugsley, C. Bréchot and J. Savall for their support; T. Hieu, C. Soto, E. Bourreterre and B. Faye for technical assistance; Z. Szabó, D. Tremblay for providing isolates; L.R. Hiltzik, N. Baldwin and C. Mackenzie for their searches of the archives; M. Toucas, H. d'Hauteville, E. Aldová, S. Formal, and A.T. Maurelli for information about isolates; D. Nedelec for discussion, I. Gut, M. Gut, L. Ma, D. Harris, K. Oliver and the sequencing teams at the Institut Pasteur and Wellcome Trust Sanger Institute for sequencing the samples. The views expressed in this publication are those of the authors and do not reflect the views of the US Department of the Army or Department of Defense. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Author notes

  1. Elisabeth Njamkepo, Nizar Fawal and Alicia Tran-Dien: These authors contributed equally to this work.

Affiliations

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

    Elisabeth Njamkepo, Nizar Fawal, Alicia Tran-Dien, Marie Accou-Demartin, Isabelle Carle, Monique Lejay-Collin, Simon Le Hello, Corinne Ruckly, Malika Gouali, Francine Grimont, Patrick A. D. Grimont & François-Xavier Weill

  2. Centre for Systems Genomics, University of Melbourne, Parkville, 3010, Victoria, Australia

    Jane Hawkey & Kathryn E. Holt

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

    Jane Hawkey & Kathryn E. Holt

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

    Jane Hawkey

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

    Nancy Strockbine

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

    Claire Jenkins

  7. icddr,b, Enteric and Food Microbiology Laboratory, Dhaka 1212, Bangladesh

    Kaisar A. Talukder

  8. Institut Pasteur de Bangui, BP 923, Bangui, République Centrafricaine

    Raymond Bercion

  9. Institut Pasteur de Dakar, BP 220, Dakar, Senegal

    Raymond Bercion & Amy Gassama Sow

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

    Konstantin Kuleshov, Alexander Podkolzin & German A. Shipulin

  11. Czech National Collection of Type Cultures (CNCTC), National Institute of Public Health, Prague 10, Czech Republic

    Renáta Kolínská & Helena Žemličková

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

    Julie E. Russell

  13. Pasteur Institute of St Petersburg, St Petersburg 197101, Russia

    Lidia Kaftyreva, Svetlana Egorova & Mariia Makarova

  14. Department of Medical Microbiology, University of KwaZulu-Natal, Durban 4041, South Africa

    Andreas Karas

  15. Department of Microbiology, LHUB-ULB, Brussels University Hospitals Laboratory, 1000 Brussels, Belgium

    Olivier Vandenberg

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

    Olivier Vandenberg

  17. Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK

    Alison E. Mather, Andrew J. Page, Martin Aslett, Simon R. Harris, Julian Parkhill, Nicholas R. Thomson & François-Xavier Weill

  18. Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK

    Alison E. Mather

  19. Armed Forces Research Institute of Medical Sciences (AFRIMS), Bangkok 10400, Thailand

    Carl J. Mason & Ladaporn Bodhidatta

  20. National Institute of Cholera and Enteric Diseases (NICED), Kolkata, 700010, West Bengal, India

    Thandavarayan Ramamurthy & Gururaja P. Pazhani

  21. Institut Pasteur, Collection de l'Institut Pasteur (CIP), 75724 Paris Cedex 15, France

    Chantal Bizet & Dominique Clermont

  22. Polish Collection of Microorganisms, Institute of Immunology and Experimental Therapy, 53-114 Wroclaw, Poland

    Andrzej Gamian & Agnieszka Korzeniowska-Kowal

  23. Institut Pasteur, Plate-forme Génomique (PF1), 75724 Paris Cedex 15, France

    Christiane Bouchier

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

    Astrid Louise Wester

  25. Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroon

    Marie-Christine Fonkoua & Antoinette Ngandjio

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

    Martin J. Blaser & Guillermo Perez-Perez

  27. Public Health Agency of Sweden, 17182 Solna, Sweden

    Cecilia Jernberg

  28. Biology Department and Infection Control Unit, Bégin Military Hospital, 94160 Saint-Mandé, France

    Audrey Mérens

  29. Epicentre, 75011 Paris, France

    Anne-Laure Page & Céline Langendorf

  30. Institut für Hygiene und Umwelt, 20539 Hamburg, Germany

    Peter Roggentin

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

    Angelika Fruth

  32. INSERM, IAME, UMR 1137, Univ. Paris Diderot, IAME, UMR 1137, Sorbonne Paris Cité, 75018 Paris, France

    Erick Denamur

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

    Malabi Venkatesan

  34. Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem 91120, Israel

    Hervé Bercovier

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

    Chien-Shun Chiou

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

    Bianca Colonna

  37. Central Laboratories, Ministry of Health, Jerusalem 91342, Israel

    Analia V. Ezernitchi

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

    Ghislaine Guigon & Sylvain Brisse

  39. Department of Bacteriology I, National Institute of Infectious Diseases, Tokyo, 162-8640, Japan

    Hidemasa Izumiya

  40. Department of Sera and Vaccines Evaluation, National Institute of Public Health–National Institute of Hygiene, 00-791 Warsaw, Poland

    Anna Lutyńska

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

    Monika Marejková

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

    Lorea A.M. Peterson

  43. Institut Pasteur, Bioinformatics platform, 75724 Paris Cedex 15, France

    Erika Souche

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

    Changyun Ye

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

    Helena Žemličková

  46. Hungarian National Collection of Medical Bacteria, National Center for Epidemiology, H-1097 Budapest, Hungary

    Mária Herpay

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

    Philippe Sansonetti

  48. Institut Pasteur, Microbial Evolutionary Genomics Unit, 75724 Paris Cedex 15, France

    Sylvain Brisse

  49. CNRS, UMR 3525, 75015 Paris, France

    Sylvain Brisse

  50. London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK

    Nicholas R. Thomson

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  1. Elisabeth Njamkepo
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  2. Nizar Fawal
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Contributions

R.B., P.A.D.G., S.B., N.R.T. and F.-X.W. designed the study. N.S., C.J., K.A.T., R.B., K.K., R.K., J.E.R., L.K., A.K., O.V., C.J.M., T.R., C. Bizet, A.G.S., A.G., A.L.W., M.-C.F., S.L.H., M.J.B., C.J., A.M., A.-L.P., P.R., A.F., E.D., M.V., H.B., M.H., P.A.D.G., P.S., L.B., C.-S.C., D.C., B.C., S.E., G.P.P., A.V.E., H.I., A.K.-K., A.L., M.G., F.G., C.L., M.M., L.A.M.P., G.P.-P., A.P., G.A.S., D.T., C.Y., H.Z., P.S. and F.-X.W. selected and provided characterized isolates and their epidemiological information. E.N., M.L.-C., I.C., C.R., A.T.-D., M.A.-D. and L.B. did the phenotypic experiments and DNA extractions. A.E.M. and S.R.H. provided guidance for genomic analyses. C. Bouchier performed the whole-genome sequencing. M.A. processed the short reads. E.N., N.F., K.K., S.B., K.E.H., J.H., A.J.P., G.G., E.S. and F.-X.W. analysed the genomic sequence data. F.-X.W. wrote the manuscript with major contributions from A.E.M., P.A.D.G., E.D., J.P., P.S., K.E.H., S.B. and N.R.T. All authors contributed to manuscript editing. F.-X.W. oversaw the project.

Corresponding author

Correspondence to François-Xavier Weill.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1-16, Table 3, Discussion and References (PDF 4476 kb)

Supplementary Table 1

Details of Shigella dysenteriae type 1 isolates and genomes used in this study. (XLSX 181 kb)

Supplementary Table 2

Whole-genome sequences, SNPs and phylogenetic data used in this study. (XLSX 15396 kb)

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Njamkepo, E., Fawal, N., Tran-Dien, A. et al. Global phylogeography and evolutionary history of Shigella dysenteriae type 1. Nat Microbiol 1, 16027 (2016). https://doi.org/10.1038/nmicrobiol.2016.27

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