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)

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: Penades, Prof Jose R and Roszak, Dr Aleksander and Fillol Salom, Mr Alfred and Bacarizo Roa, Dr Julio Luis and Cogdell, Professor Richard and Alqasmi, Mohammed Hussein H
• 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 > School of Infection & Immunity
• 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

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
66077	2	Molecular biology of the PICIs, a novel and widespread family of mobile genetic elements involved in bacterial virulence	Jose R Penades	Medical Research Council (MRC)	MR/M003876/1	RI INFECTION IMMUNITY & INFLAMMATION
69378	1	Understanding a novel mechanim involving pathogenity islands in the transfer of unlinked chromosomal virulence genes	Jose R Penades	Biotechnology and Biological Sciences Research Council (BBSRC)	BB/N002873/1	RI INFECTION IMMUNITY & INFLAMMATION
302971	0	Helper and satellite pathogenicity islands: the discovery of two novel subcellular elements with a huge impact on bacterial pathogenesis and evolution	Jose R Penades	Biotechnology and Biological Sciences Research Council (BBSRC)	BB/S003835/1	III - Bacteriology
72724	1	Understanding bacterial host adaptation to combat infectious diseases	Jose R Penades	Wellcome Trust (WELLCOTR)	201531/Z/16/Z	RI INFECTION IMMUNITY & INFLAMMATION
68770	1	DUT-Signal	Jose R Penades	European Research Council (ERC)	670932	RI INFECTION IMMUNITY & INFLAMMATION