Global phylogeography and evolutionary history of Shigella dysenteriae type 1

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.

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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.

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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.

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Correspondence to François-Xavier Weill.

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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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