Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors

Fillol-Salom, A., Rostøl, J. T., Ojiogu, A. D., Chen, J., Douce, G. , Humphrey, S. and Penadés, J. R. (2022) Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors. Cell, 185(17), 3248-3262.e20. (doi: 10.1016/j.cell.2022.07.014) (PMID:35985290)

Abstract

Bacteria encode sophisticated anti-phage systems that are diverse and versatile and display high genetic mobility. How this variability and mobility occurs remains largely unknown. Here, we demonstrate that a widespread family of pathogenicity islands, the phage-inducible chromosomal islands (PICIs), carry an impressive arsenal of defense mechanisms, which can be disseminated intra- and inter-generically by helper phages. These defense systems provide broad immunity, blocking not only phage reproduction, but also plasmid and non-cognate PICI transfer. Our results demonstrate that phages can mobilize PICI-encoded immunity systems to use them against other mobile genetic elements, which compete with the phages for the same bacterial hosts. Therefore, despite the cost, mobilization of PICIs may be beneficial for phages, PICIs, and bacteria in nature. Our results suggest that PICIs are important players controlling horizontal gene transfer and that PICIs and phages establish mutualistic interactions that drive bacterial ecology and evolution.

• Item Type: Articles
• Additional Information: This work was supported by grants MR/M003876/1, MR/V000772/1, and MR/S00940X/1 from the Medical Research Council (UK); BB/N002873/1, BB/V002376/1, and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK); ERC-ADG-2014 Proposal n° 670932 Dut-signal (from EU); and Wellcome Trust 201531/Z/16/Z to J.R.P. J.T.R. was supported by EMBO Postdoctoral Fellowship ALTF 164-2021.
• Keywords: PICI, Immune System, Bacteriophages - genetics, Plasmids, Gene Transfer, Horizontal, horizontal gene transfer, Genomic Islands, defense islands, Bacteria - genetics, mobile genetic elements, bacteriophage
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Douce, Dr Gillian and Penades, Prof Jose R and Ojiogu, Miss Adaeze
• Authors: Fillol-Salom, A., Rostøl, J. T., Ojiogu, A. D., Chen, J., Douce, G., Humphrey, S., and Penadés, J. R.
• College/School: College of Medical Veterinary and Life Sciences > School of Infection & Immunity
• Journal Name: Cell
• Publisher: Elsevier (Cell Press)
• ISSN: 0092-8674
• ISSN (Online): 1097-4172
• Published Online: 18 August 2022
• Copyright Holders: Copyright © 2022 Elsevier Inc.
• First Published: First published in Cell 185(17): 3248-3262.e20
• Publisher Policy: Reproduced in accordance with the publisher copyright policy

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
170721		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	III - Bacteriology - Dr J Penades
172242		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	Institute of Infection, Immunity & Inflammation
302971		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
173671		Prof. R. Fitzgerald. Wellcome Trust Award 201531/Z/16/Z - Understanding bacterial host adaptation to combat infectious diseases	Jose R Penades	Wellcome Trust (WELLCOTR)	R44516 - WT 201531/Z/16/Z	Institute of Infection, Immunity & Inflammation