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Hijacking the hijackers: Escherichia coli pathogenicity islands redirect helper phage packaging for their own benefit

DOI: 10.1016/j.molcel.2019.06.017 DOI Help

Authors: Alfred Fillol-salom (University of Glasgow) , Julio Bacarizo (University of Glasgow) , Mohammed Alqasmi (University of Glasgow; Shaqra University) , J. Rafael Ciges-tomas (Instituto de Biomedicina de Valencia (IBV-CSIC); CIBER de Enfermedades Raras (CIBERER)) , Roser Martínez-rubio (Universidad CEU Cardenal Herrera) , Aleksander W. Roszak (University of Glasgow) , Richard J. Cogdell (University of Glasgow) , John Chen (National University of Singapore) , Alberto Marina (Instituto de Biomedicina de Valencia (CSIC); CIBER de Enfermedades Raras (CIBERER)) , José R. Penadés (University of Glasgow; MRC–University of Glasgow Centre for Virus Research)
Co-authored by industrial partner: No

Type: Journal Paper
Journal: Molecular Cell

State: Published (Approved)
Published: July 2019
Diamond Proposal Number(s): 16258 , 20229

Open Access Open Access

Abstract: Phage-inducible chromosomal islands (PICIs) represent a novel and universal class of mobile genetic elements, which have broad impact on bacterial virulence. In spite of their relevance, how the Gram-negative PICIs hijack the phage machinery for their own specific packaging and how they block phage reproduction remains to be determined. Using genetic and structural analyses, we solve the mystery here by showing that the Gram-negative PICIs encode a protein that simultaneously performs these processes. This protein, which we have named Rpp (for redirecting phage packaging), interacts with the phage terminase small subunit, forming a heterocomplex. This complex is unable to recognize the phage DNA, blocking phage packaging, but specifically binds to the PICI genome, promoting PICI packaging. Our studies reveal the mechanism of action that allows PICI dissemination in nature, introducing a new paradigm in the understanding of the biology of pathogenicity islands and therefore of bacterial pathogen evolution.

Journal Keywords: bacteriophage; pathogenicity islands; pirating; PICI; evolution; virulence; gene transfer; transduction; TerS

Subject Areas: Biology and Bio-materials

Instruments: I04-Macromolecular Crystallography