Enhanced virulence and stress tolerance are signatures of epidemiologically successful Shigella sonnei

Sydney L. Miles, Dilys Santillo, Hannah Painter, Kathryn Wright, Vincenzo Torraca, Ana T. López-Jiménez, Mollie Virgo, Xosé M. Matanza, Abigail Clements, Claire Jenkins, Stephen Baker, Kate S. Baker, David Cisneros, Andrea Puhar, Vanessa Sancho-Shimizu, Kathryn E. Holt and Serge Mostowy ()
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Sydney L. Miles: London School of Hygiene and Tropical Medicine
Dilys Santillo: Imperial College London
Hannah Painter: London School of Hygiene and Tropical Medicine
Kathryn Wright: London School of Hygiene and Tropical Medicine
Vincenzo Torraca: London School of Hygiene and Tropical Medicine
Ana T. López-Jiménez: London School of Hygiene and Tropical Medicine
Mollie Virgo: London School of Hygiene and Tropical Medicine
Xosé M. Matanza: Imperial College London
Abigail Clements: Imperial College London
Claire Jenkins: UK Health Security Agency
Stephen Baker: Biopolis
Kate S. Baker: University of Cambridge
David Cisneros: Queen’s University Belfast
Andrea Puhar: Queen’s University Belfast
Vanessa Sancho-Shimizu: Imperial College London
Kathryn E. Holt: London School of Hygiene and Tropical Medicine
Serge Mostowy: London School of Hygiene and Tropical Medicine

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract Shigellosis is a leading cause of diarrhoeal deaths, with Shigella sonnei increasingly implicated as a dominant agent. S. sonnei is divided into five monophyletic lineages, yet most infections are caused by a few clonal sub-lineages within Lineage 3 that are quite distinct from the widely used Lineage 2 laboratory strain 53G. Factors underlying the success of these globally dominant lineages remain unclear in part due to a lack of complete genome sequences and animal models. Here, we utilise a novel reference collection of representative Lineage 1, 2 and 3 isolates and find that epidemiologically successful S. sonnei harbour fewer genes encoding putative immunogenic components whilst key virulence-associated regions (including the type three secretion system and O-antigen) remain highly conserved. Using a zebrafish infection model, Lineage 3 isolates proved most virulent, driven by increased dissemination and a greater neutrophil response. These isolates also show increased resistance to complement-mediated killing alongside upregulated expression of group four capsule synthesis genes. Consistently, primary human neutrophil infections revealed an increased tolerance to phagosomal killing. Together, our findings link the epidemiological success of S. sonnei to heightened virulence and stress tolerance, and highlight zebrafish as a valuable platform to illuminate factors underlying establishment of epidemiological success.

Date: 2025
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DOI: 10.1038/s41467-025-64057-y

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