Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22

Fillol-Salom, A. , Bacigalupe, R., Humphrey, S. , Chiang, Y. N., Chen, J. and Penadés, J. R. (2021) Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22. Nature Communications, 12, 6510. (doi: 10.1038/s41467-021-26520-4) (PMID:34751192) (PMCID:PMC8575938)

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Abstract

Lysogenic induction ends the stable association between a bacteriophage and its host, and the transition to the lytic cycle begins with early prophage excision followed by DNA replication and packaging (ERP). This temporal program is considered universal for P22-like temperate phages, though there is no direct evidence to support the timing and sequence of these events. Here we report that the long-standing ERP program is an observation of the experimentally favored Salmonella phage P22 tsc229 heat-inducible mutant, and that wild-type P22 actually follows the replication-packaging-excision (RPE) program. We find that P22 tsc229 excises early after induction, but P22 delays excision to just before it is detrimental to phage production. This allows P22 to engage in lateral transduction. Thus, at minimal expense to itself, P22 has tuned the timing of excision to balance propagation with lateral transduction, powering the evolution of its host through gene transfer in the interest of self-preservation.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Penades, Prof Jose R and Fillol Salom, Mr Alfred and Humphrey, Dr Suzie
Authors: Fillol-Salom, A., Bacigalupe, R., Humphrey, S., Chiang, Y. N., Chen, J., and Penadés, J. R.
College/School:College of Medical Veterinary and Life Sciences > School of Infection & Immunity
Journal Name:Nature Communications
Publisher:Nature Research
ISSN:2041-1723
ISSN (Online):2041-1723
Copyright Holders:Copyright © 2021 The Authors
First Published:First published in Scientific Reports 12: 6510
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
170721Molecular biology of the PICIs, a novel and widespread family of mobile genetic elements involved in bacterial virulenceJose R PenadesMedical Research Council (MRC)MR/M003876/1III - Bacteriology - Dr J Penades
304055Deciphering Gram-negative phage-inducible chromosomal island strategies for spreading in natureJose R PenadesMedical Research Council (MRC)MRS00940X/1III - Bacteriology
172242Understanding a novel mechanim involving pathogenity islands in the transfer of unlinked chromosomal virulence genesJose R PenadesBiotechnology and Biological Sciences Research Council (BBSRC)BB/N002873/1Institute of Infection, Immunity & Inflammation
302971Helper 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
172321DUT-SignalJose R PenadesEuropean Research Council (ERC)670932Institute of Infection, Immunity & Inflammation
173671Prof. R. Fitzgerald. Wellcome Trust Award 201531/Z/16/Z - Understanding bacterial host adaptation to combat infectious diseasesJose R PenadesWellcome Trust (WELLCOTR)R44516 - WT 201531/Z/16/ZInstitute of Infection, Immunity & Inflammation