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

Fillol-Salom, A., Bacarizo Roa, J. L., Alqasmi, M. H. H., Ciges-Tomas, J. R., Martínez-Rubio, R., Roszak, A. W., Cogdell, R. J. , Chen, J., Marina, A. and Penades, J. R. (2019) Hijacking the hijackers: Escherichia coli pathogenicity islands redirect helper phage packaging for their own benefit. Molecular Cell, 75(5), 1020-1030.e4. (doi: 10.1016/j.molcel.2019.06.017) (PMID:31350119) (PMCID:PMC6739421)

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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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Cogdell, Professor Richard and Alqasmi, Mohammed Hussein H and Penades, Professor Jose R and Bacarizo Roa, Dr Julio Luis and Roszak, Dr Aleksander and Fillol Salom, Mr Alfred
Authors: Fillol-Salom, A., Bacarizo Roa, J. L., Alqasmi, M. H. H., Ciges-Tomas, J. R., Martínez-Rubio, R., Roszak, A. W., Cogdell, R. J., Chen, J., Marina, A., and Penades, J. R.
College/School:College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:Molecular Cell
Publisher:Elsevier (Cell Press)
ISSN:1097-2765
ISSN (Online):1097-4164
Published Online:23 July 2019
Copyright Holders:Copyright © 2019 The Authors
First Published:First published in Molecular Cell 75(5): 1020-1030.e4
Publisher Policy:Reproduced under a Creative Commons license

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
660772Molecular biology of the PICIs, a novel and widespread family of mobile genetic elements involved in bacterial virulenceJose R PenadesMedical Research Council (MRC)MR/M003876/1RI INFECTION IMMUNITY & INFLAMMATION
693781Understanding a novel mechanim involving pathogenity islands in the transfer of unlinked chromosomal virulence genesJose R PenadesBiotechnology and Biological Sciences Research Council (BBSRC)BB/N002873/1RI INFECTION IMMUNITY & INFLAMMATION
3029710Helper and satellite pathogenicity islands: the discovery of two novel subcellular elements with a huge impact on bacterial pathogenesis and evolutionJose R PenadesBiotechnology and Biological Sciences Research Council (BBSRC)BB/S003835/1III - Bacteriology
727241Understanding bacterial host adaptation to combat infectious diseasesJose R PenadesWellcome Trust (WELLCOTR)201531/Z/16/ZRI INFECTION IMMUNITY & INFLAMMATION
687701DUT-SignalJose R PenadesEuropean Research Council (ERC)670932RI INFECTION IMMUNITY & INFLAMMATION