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Open Access Research article

Genomic analysis of the emergence of 20th century epidemic dysentery

Laurence Rohmer1*, Michael A Jacobs1, Mitchell J Brittnacher1, Christine Fong1, Hillary S Hayden1, Didier Hocquet23, Eli J Weiss1, Matthew Radey1, Yves Germani4, Kaisar Ali Talukder5, Anthony J Hager1, John M Kemner1, Elizabeth H Sims-Day1, Susana Matamouros1, Kyle R Hager1 and Samuel I Miller167

Author Affiliations

1 Department of Microbiology, University of Washington, Seattle, WA, USA

2 Hygiène Hospitalière, University Hospital of Besançon, Besançon, France

3 UMR6249 Chrono-Environnement, Université de Franche-Comté, Besançon, France

4 Institut Pasteur, Paris, France

5 International Centre for Diarrheal Disease Research, Dhaka, Bangladesh

6 Department of Genome Sciences, University of Washington, Seattle, WA, USA

7 Department of Medicine, University of Washington, Seattle, WA, USA

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BMC Genomics 2014, 15:355  doi:10.1186/1471-2164-15-355

Published: 10 May 2014

Abstract

Background

Shigella dysenteriae type 1 (Sd1) causes recurrent epidemics of dysentery associated with high mortality in many regions of the world. Sd1 infects humans at very low infectious doses (10 CFU), and treatment is complicated by the rapid emergence of antibiotic resistant Sd1 strains. Sd1 is only detected in the context of human infections, and the circumstances under which epidemics emerge and regress remain unknown.

Results

Phylogenomic analyses of 56 isolates collected worldwide over the past 60 years indicate that the Sd1 clone responsible for the recent pandemics emerged at the turn of the 20th century, and that the two world wars likely played a pivotal role for its dissemination. Several lineages remain ubiquitous and their phylogeny indicates several recent intercontinental transfers. Our comparative genomics analysis reveals that isolates responsible for separate outbreaks, though closely related to one another, have independently accumulated antibiotic resistance genes, suggesting that there is little or no selection to retain these genes in-between outbreaks. The genomes appear to be subjected to genetic drift that affects a number of functions currently used by diagnostic tools to identify Sd1, which could lead to the potential failure of such tools.

Conclusions

Taken together, the Sd1 population structure and pattern of evolution suggest a recent emergence and a possible human carrier state that could play an important role in the epidemic pattern of infections of this human-specific pathogen. This analysis highlights the important role of whole-genome sequencing in studying pathogens for which epidemiological or laboratory investigations are particularly challenging.

Keywords:
Shigella dysenteriae; Dysentery; Genome evolution; Phylogeny; Antibiotic resistance; Genomic adaptation; Human carrier; Pandemic