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The novel anti-phage system Shield co-opts an RmuC domain to mediate phage defense across Pseudomonas species

Macdonald, E.; Wright, R.; Connolly, J.P.R.; Strahl, H.; Brockhurst, M.; van Houte, S.; Blower, T.R.; Palmer, T.; Mariano, G.

The novel anti-phage system Shield co-opts an RmuC domain to mediate phage defense across Pseudomonas species Thumbnail


Authors

E. Macdonald

R. Wright

J.P.R. Connolly

H. Strahl

M. Brockhurst

S. van Houte

T. Palmer

G. Mariano



Abstract

Competitive bacteria-bacteriophage interactions have resulted in the evolution of a plethora of bacterial defense systems preventing phage propagation. In recent years, computational and bioinformatic approaches have underpinned the discovery of numerous novel bacterial defense systems. Anti-phage systems are frequently encoded together in genomic loci termed defense islands. Here we report the identification and characterisation of a novel anti-phage system, that we have termed Shield, which forms part of the Pseudomonas defensive arsenal. The Shield system comprises the core component ShdA, a membrane-bound protein harboring an RmuC domain. Heterologous production of ShdA alone is sufficient to mediate bacterial immunity against several phages. We demonstrate that Shield and ShdA confer population-level immunity and that they can also decrease transformation efficiency. We further show that ShdA homologues can degrade DNA in vitro and, when expressed in a heterologous host, can alter the organisation of the host chromosomal DNA. Use of comparative genomic approaches identified how Shield can be divided into four subtypes, three of which contain additional components that in some cases can negatively affect the activity of ShdA and/or provide additional lines of phage defense. Collectively, our results identify a new player within the Pseudomonas bacterial immunity arsenal that displays a novel mechanism of protection, and reveals a role for RmuC domains in phage defense.

Citation

Macdonald, E., Wright, R., Connolly, J., Strahl, H., Brockhurst, M., van Houte, S., Blower, T., Palmer, T., & Mariano, G. (2023). The novel anti-phage system Shield co-opts an RmuC domain to mediate phage defense across Pseudomonas species. PLoS Genetics, 19(6), Article e1010784. https://doi.org/10.1371/journal.pgen.1010784

Journal Article Type Article
Acceptance Date May 12, 2023
Online Publication Date Jun 5, 2023
Publication Date 2023-06
Deposit Date Jun 19, 2023
Publicly Available Date Jun 19, 2023
Journal PLOS Genetics
Print ISSN 1553-7390
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 19
Issue 6
Article Number e1010784
DOI https://doi.org/10.1371/journal.pgen.1010784
Public URL https://durham-repository.worktribe.com/output/1171465

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Publisher Licence URL
http://creativecommons.org/licenses/by/4.0/

Copyright Statement
© 2023 Macdonald et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.






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