A widespread family of phage-inducible chromosomal islands only steals bacteriophage tails to spread in nature

Alqurainy, N., Miguel-Romero, L., Moura de Sousa, J., Chen, J., Rocha, E. P.C., Fillol-Salom, A. and Penadés, J. R. (2023) A widespread family of phage-inducible chromosomal islands only steals bacteriophage tails to spread in nature. Cell Host and Microbe, 31(1), 69-82.e5. (doi: 10.1016/j.chom.2022.12.001) (PMID:36596306)

Abstract

Phage satellites are genetic elements that couple their life cycle to that of helper phages they parasitize, interfering with phage packaging through the production of small capsids, where only satellites are packaged. So far, in all analyzed systems, the satellite-sized capsids are composed of phage proteins. Here, we report that a family of phage-inducible chromosomal islands (PICIs), a type of satellites, encodes all the proteins required for both the production of small-sized capsids and the exclusive packaging of the PICIs into these capsids. Therefore, this new family, named capsid-forming PICIs (cf-PICIs), only requires phage tails to generate PICI particles. Remarkably, the representative cf-PICIs are produced with no cost from their helper phages, suggesting that the relationship between these elements is not parasitic. Finally, our phylogenomic studies indicate that cf-PICIs are present both in gram-positive and gram-negative bacteria and have evolved at least three times independently to spread in nature.

• Item Type: Articles
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Miguel Romero, Dr Laura and Penades, Prof Jose R and Fillol Salom, Mr Alfred and ALQURAINY, Nasser Khamis S
• Authors: Alqurainy, N., Miguel-Romero, L., Moura de Sousa, J., Chen, J., Rocha, E. P.C., Fillol-Salom, A., and Penadés, J. R.
• College/School: College of Medical Veterinary and Life Sciences > School of Infection & Immunity
• Journal Name: Cell Host and Microbe
• Publisher: Elsevier (Cell Press)
• ISSN: 1931-3128
• ISSN (Online): 1934-6069
• Published Online: 02 January 2023
• Copyright Holders: Copyright © 2022 The Authors
• First Published: First published in Cell Host and Microbe 31(1): 69-82.e5
• Publisher Policy: Reproduced under a Creative Commons License

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
304055		Deciphering Gram-negative phage-inducible chromosomal island strategies for spreading in nature	Jose R Penades	Medical Research Council (MRC)	MRS00940X/1	III - Bacteriology
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
172321		DUT-Signal	Jose R Penades	European Research Council (ERC)	670932	Institute of Infection, Immunity & Inflammation
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