Dual pathogenicity island transfer by piggybacking lateral transduction

Su Juan Chee, M., Serrano, E. , Ning Chiang, Y., Harling-Lee, J., Man, R., Bacigalupe, R., Ross Fitzgerald, J., Penades, J. R. and Chen, J. (2023) Dual pathogenicity island transfer by piggybacking lateral transduction. Cell, 186(16), 3414-3426.e16. (doi: 10.1016/j.cell.2023.07.001) (PMID:37541198)

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Abstract

Lateral transduction (LT) is the process by which temperate phages mobilize large sections of bacterial genomes. Despite its importance, LT has only been observed during prophage induction. Here, we report that superantigen-carrying staphylococcal pathogenicity islands (SaPIs) employ a related but more versatile and complex mechanism of gene transfer to drive chromosomal hypermobility while self-transferring with additional virulence genes from the host. We found that after phage infection or prophage induction, activated SaPIs form concatamers in the bacterial chromosome by switching between parallel genomic tracks in replication bubbles. This dynamic life cycle enables SaPIbov1 to piggyback its LT of staphylococcal pathogenicity island vSaα, which encodes an array of genes involved in host-pathogen interactions, allowing both islands to be mobilized intact and transferred in a single infective particle. Our findings highlight previously unknown roles of pathogenicity islands in bacterial virulence and show that their evolutionary impact extends beyond the genes they carry.

Item Type:Articles
Additional Information:This work was supported in part by the Singapore Ministry of Education grants MOE2017-T2-2-163 and MOE2019-T2-2-162 to J.C.; by grants MR/M003876/1, MR/V000772/1, and MR/S00940X/1 from the Medical Research Council (UK), BB/V002376/1 and BB/V009583/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), and EP/X026671/1 from the Engineering and Physical Sciences Research Council (EPSRC, UK) to J.R.P.; by Biotechnology and Biological Sciences Research Council institute strategic grant funding (ISP2) (BB/P013740/1) to J.R.F.; and by Wellcome Trust 201531/Z/16/Z to J.R.P. and J.R.F.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Penades, Prof Jose R and Serrano, Dr Ester
Authors: Su Juan Chee, M., Serrano, E., Ning Chiang, Y., Harling-Lee, J., Man, R., Bacigalupe, R., Ross Fitzgerald, J., Penades, J. R., and Chen, J.
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:03 August 2023

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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
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/ZSchool of Infection & Immunity