• An Erratum to this article was published on 01 April 2017

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Abstract

An epidemiological paradox surrounds Salmonella enterica serovar Enteritidis. In high-income settings, it has been responsible for an epidemic of poultry-associated, self-limiting enterocolitis, whereas in sub-Saharan Africa it is a major cause of invasive nontyphoidal Salmonella disease, associated with high case fatality. By whole-genome sequence analysis of 675 isolates of S. Enteritidis from 45 countries, we show the existence of a global epidemic clade and two new clades of S. Enteritidis that are geographically restricted to distinct regions of Africa. The African isolates display genomic degradation, a novel prophage repertoire, and an expanded multidrug resistance plasmid. S. Enteritidis is a further example of a Salmonella serotype that displays niche plasticity, with distinct clades that enable it to become a prominent cause of gastroenteritis in association with the industrial production of eggs and of multidrug-resistant, bloodstream-invasive infection in Africa.

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  • 24 October 2016

    In the version of this article initially published, the last name of author Lars Barquist was inadvertently duplicated. The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

This work was supported by the Wellcome Trust. We would like to thank the members of the Pathogen Informatics Team and the core sequencing teams at the Wellcome Trust Sanger Institute (Cambridge, UK). We are grateful to D. Harris for work in managing the sequence data.

This work was supported by a number of organizations. The authors from the Wellcome Trust Sanger Institute were funded by Wellcome Trust award 098051. N.A.F. was supported by Wellcome Trust research fellowship WT092152MA. N.A.F., R.S.H., and this work were supported by a strategic award from the Wellcome Trust for the MLW Clinical Research Programme (101113/Z/13/Z). The authors from the Institut Pasteur were funded by the Institut Pasteur, by the Institut de Veille Sanitaire, and by the French government 'Investissement d'Avenir' program (Integrative Biology of Emerging Infectious Diseases Laboratory of Excellence, grant ANR-10-LABX-62-IBEID). J.J. was supported by the antibiotic resistance surveillance project in the Democratic Republic of the Congo, funded by Project 2.01 of the Third Framework Agreement between the Belgian Directorate General of Development Cooperation and the Institute of Tropical Medicine (Antwerp, Belgium). S.K. was supported by NIH grant R01 AI099525-02. A.E.M. was supported by Wellcome Trust grant 098051 while at the Wellcome Trust Sanger Institute and by Biotechnology and Biological Sciences Research Council grant BB/M014088/1 at the University of Cambridge. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Author notes

    • Alison E Mather

    Present address: Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.

    • Melita A Gordon
    •  & Nicholas R Thomson

    These authors contributed equally to this work.

Affiliations

  1. Liverpool School of Tropical Medicine, Liverpool, UK.

    • Nicholas A Feasey
    •  & Christopher M Parry
  2. Wellcome Trust Sanger Institute, Cambridge, UK.

    • Nicholas A Feasey
    • , James Hadfield
    • , Gemma C Langridge
    • , Theresa Feltwell
    • , Simon R Harris
    • , Alison E Mather
    • , Maria Fookes
    • , Martin Aslett
    • , Calman A Maclennan
    • , Robert A Kingsley
    • , Julian Parkhill
    • , Gordon Dougan
    •  & Nicholas R Thomson
  3. Malawi Liverpool Wellcome Trust Clinical Research Programme, University of Malawi College of Medicine, Blantyre, Malawi.

    • Nicholas A Feasey
    • , Chisomo Msefula
    • , Robert S Heyderman
    •  & Melita A Gordon
  4. Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.

    • Nicholas A Feasey
    • , Paul Wigley
    • , Neil French
    • , Lizeth Lacharme-Lora
    • , Dean B Everett
    •  & Melita A Gordon
  5. Centre for Enteric Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.

    • Karen H Keddy
    •  & Anthony M Smith
  6. Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.

    • Karen H Keddy
  7. Gastrointestinal Bacteria Reference Unit, Public Health England, Colindale, UK.

    • Timothy J Dallman
    •  & Satheesh Nair
  8. Institute of Tropical Medicine, Antwerp, Belgium.

    • Jan Jacobs
  9. Department of Microbiology and Immunology, University of Leuven, Leuven, Belgium.

    • Jan Jacobs
  10. Center for Food Safety, Department of Food Science and Technology, University of Georgia, Athens, Georgia, USA.

    • Xiangyu Deng
  11. Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

    • Xiangyu Deng
  12. Institute for Molecular Infection Biology, University of Würzburg, Würzburg, Germany.

    • Lars Barquist
  13. University of Malawi College of Medicine, Blantyre, Malawi.

    • Chisomo Msefula
  14. Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya.

    • Samuel Kariuki
    •  & Robert S Onsare
  15. Jenner Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK.

    • Calman A Maclennan
  16. Institut Pasteur, Paris, France.

    • François-Xavier Weill
    •  & Simon Le Hello
  17. Department of Microbiology and Molecular Genetics, University of California–Irvine, Irvine, California, USA.

    • Michael McClelland
    •  & Prerak Desai
  18. London School of Hygiene and Tropical Medicine, London, UK.

    • Christopher M Parry
    •  & Nicholas R Thomson
  19. School of Tropical Medicine and Global Health, Nagasaki University, Nagasaki, Japan.

    • Christopher M Parry
  20. Department of Epidemiology and Population Health, University of Liverpool, Liverpool, UK.

    • John Cheesbrough
  21. Enteropathogen Division, Administración Nacional de Laboratorios e Institutos de Salud (ANLIS), Carlos G. Malbran Institute, Buenos Aires, Argentina.

    • Josefina Campos
  22. Instituto de Higiene, Facultad de Medicina, Universidad de la Republica, Montevideo, Uruguay.

    • Jose A Chabalgoity
    •  & Laura Betancor
  23. Antimicrobial Resistance and Healthcare-Associated Infections Reference Unit, Public Health England, Colindale, UK.

    • Katie L Hopkins
  24. Swansea Medical School, Swansea University, Swansea, UK.

    • Tom J Humphrey
  25. National Institute of Biomedical Research, Kinshasa, Democratic Republic of the Congo.

    • Octavie Lunguya
  26. University Hospital of Kinshasa, Kinshasa, Democratic Republic of the Congo.

    • Octavie Lunguya
  27. School of Veterinary Sciences, University of Bristol, Bristol, UK.

    • Tristan A Cogan
  28. Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland, USA.

    • Milagritos D Tapia
    • , Sharon M Tennant
    • , Kristin Bornstein
    •  & Myron M Levine
  29. Centre pour le Développement des Vaccins, Bamako, Mali.

    • Samba O Sow
  30. Institute of Food Research, Colney, Norwich, UK.

    • Robert A Kingsley
  31. Division of Infection and Immunity, University College London, London, UK.

    • Robert S Heyderman

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Contributions

Study design: N.A.F., N.R.T., M.A.G., G.D., R.A.K., and J.P. Data analysis: N.A.F., N.R.T., J.H., T.J.D., T.F., L.B.B., P.W., L.L.-L., G.C.L., S.R.H., A.E.M., M.F., and M.A. Isolate acquisition and processing, and clinical data collection: N.A.F., K.H.K., J.J., X.D., C.M., S.K., C.A.M., R.S.O., F.-X.W., S.L.H., A.M.S., M.M., P.D., C.M.P., J. Cheesbrough, N.F., J. Campos, J.A.C., L.B., K.L.H., S.N., T.J.H., O.L., T.A.C., M.D.T., S.O.S., S.M.T., K.B., M.M.L., D.B.E., and R.S.H. Manuscript writing: N.A.F., J.H., N.R.T., and M.A.G. All authors contributed to manuscript editing.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Nicholas A Feasey.

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