The assembly of a hybrid type IV secretion system by a Crohn’s disease-associated Escherichia coli strain

Jonas Wong, Ahmad Refaat, Pablo Villacampa-Teixeira, Jonasz B. Patkowski, Natalie Lapa, Julian Ortiz, Kasia Dzierlega, Blake Roberts, Stephanie Tollenaar, Matthew Croxen, Aducio Thiesen, Dina Kao, Ben Willing, Xavier Clemente-Casares, Tiago R. D. Costa () and Wael Elhenawy ()
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Jonas Wong: University of Alberta
Ahmad Refaat: University of Alberta
Pablo Villacampa-Teixeira: Imperial College London
Jonasz B. Patkowski: Imperial College London
Natalie Lapa: University of Alberta
Julian Ortiz: University of Alberta
Kasia Dzierlega: University of Alberta
Blake Roberts: University of Alberta
Stephanie Tollenaar: University of Alberta
Matthew Croxen: Li Ka Shing Institute of Virology
Aducio Thiesen: University of Alberta
Dina Kao: University of Alberta
Ben Willing: University of Alberta
Xavier Clemente-Casares: University of Alberta
Tiago R. D. Costa: Imperial College London
Wael Elhenawy: University of Alberta

Nature Communications, 2025, vol. 16, issue 1, 1-17

Abstract: Abstract Type IV secretion systems (T4SSs) are central to bacterial pathogenesis. Traditionally known for facilitating DNA transfer via conjugation, T4SSs also mediate biofilm formation. These biofilms are critical for the fitness of adherent-invasive Escherichia coli (AIEC), which are commonly isolated from Crohn’s disease patients and are known for propelling gut inflammation. Many AIEC strains carry F-like plasmids encoding the IncF subgroup of T4SSs. Unlike minimized systems with 12 core components, the IncF family is an expanded T4SS with additional genes that enhance conjugation. Here, we show that a biofilm-forming AIEC strain harbors an unusual IncF plasmid that lacks two conserved components essential for T4SS functionality. This strain forms a natural hybrid T4SS where the missing components are supplied by a co-residing chromosomal T4SS on an integrative and conjugative element (ICE). Biochemical assays reveal that this hybrid T4SS drives pilin polymerization and biofilm formation on epithelial cells. Furthermore, we show that a bacterial subpopulation expresses the IncF and ICE-encoded genes in response to host cells, leading to the assembly of biofilms and enhanced fitness in the gut. These findings uncover crosstalk between two evolutionary distant mobile genetic elements to form a hybrid T4SS that mediates biofilm biogenesis by a Crohn’s disease-associated pathogen.

Date: 2025
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DOI: 10.1038/s41467-025-63859-4

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