A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.

Bacteriophages must hijack the gene expression machinery of their bacterial host to efficiently replicate. Recently, we have shown that the early-expressed protein gp014 of Pseudomonas nucleus-forming phage phiKZ forms a stable complex with the host ribosomes and modulates the overall protein expres...

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Main Authors: Wichanan Wannasrichan, Sucheewin Krobthong, Chase J Morgan, Emily G Armbruster, Milan Gerovac, Yodying Yingchutrakul, Patompon Wongtrakoongate, Jörg Vogel, Chanat Aonbangkhen, Poochit Nonejuie, Joe Pogliano, Vorrapon Chaikeeratisak
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-02-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012936
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author Wichanan Wannasrichan
Sucheewin Krobthong
Chase J Morgan
Emily G Armbruster
Milan Gerovac
Yodying Yingchutrakul
Patompon Wongtrakoongate
Jörg Vogel
Chanat Aonbangkhen
Poochit Nonejuie
Joe Pogliano
Vorrapon Chaikeeratisak
author_facet Wichanan Wannasrichan
Sucheewin Krobthong
Chase J Morgan
Emily G Armbruster
Milan Gerovac
Yodying Yingchutrakul
Patompon Wongtrakoongate
Jörg Vogel
Chanat Aonbangkhen
Poochit Nonejuie
Joe Pogliano
Vorrapon Chaikeeratisak
author_sort Wichanan Wannasrichan
collection DOAJ
description Bacteriophages must hijack the gene expression machinery of their bacterial host to efficiently replicate. Recently, we have shown that the early-expressed protein gp014 of Pseudomonas nucleus-forming phage phiKZ forms a stable complex with the host ribosomes and modulates the overall protein expression profile during phage infection. Here, we discover a nucleus-forming phage, designated Churi, that is closely related to phiKZ. Churi encodes gp335, a homolog of gp014-phiKZ, which is expressed during the early stages of infection, and its overexpression in bacterial cells interferes with bacterial growth, suggesting its role in phage-host interplay. We predict experimentally that gp335 also interacts with host ribosomal proteins, similar to its homolog gp014-phiKZ, thereby strengthening its involvement in protein translation during phage infection. We further show that GFP-tagged gp335 specifically localizes by clustering around the phage nucleus and remains associated with it throughout the infection cycle. The CRISPR-Cas13-mediated deletion of gp335 reveals that the mutant phage fails to replicate efficiently, resulting in an extended latent period. Altogether, our study demonstrates that gp335 is an early-expressed protein of the Chimallivirus Churi that localizes in proximity to the phage nucleus, likely serving a role in localized translation to ensure efficient phage propagation.
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issn 1553-7366
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spelling doaj-art-2699bb38b8894614b83448f82cd3dbdd2025-08-20T02:15:20ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-02-01212e101293610.1371/journal.ppat.1012936A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.Wichanan WannasrichanSucheewin KrobthongChase J MorganEmily G ArmbrusterMilan GerovacYodying YingchutrakulPatompon WongtrakoongateJörg VogelChanat AonbangkhenPoochit NonejuieJoe PoglianoVorrapon ChaikeeratisakBacteriophages must hijack the gene expression machinery of their bacterial host to efficiently replicate. Recently, we have shown that the early-expressed protein gp014 of Pseudomonas nucleus-forming phage phiKZ forms a stable complex with the host ribosomes and modulates the overall protein expression profile during phage infection. Here, we discover a nucleus-forming phage, designated Churi, that is closely related to phiKZ. Churi encodes gp335, a homolog of gp014-phiKZ, which is expressed during the early stages of infection, and its overexpression in bacterial cells interferes with bacterial growth, suggesting its role in phage-host interplay. We predict experimentally that gp335 also interacts with host ribosomal proteins, similar to its homolog gp014-phiKZ, thereby strengthening its involvement in protein translation during phage infection. We further show that GFP-tagged gp335 specifically localizes by clustering around the phage nucleus and remains associated with it throughout the infection cycle. The CRISPR-Cas13-mediated deletion of gp335 reveals that the mutant phage fails to replicate efficiently, resulting in an extended latent period. Altogether, our study demonstrates that gp335 is an early-expressed protein of the Chimallivirus Churi that localizes in proximity to the phage nucleus, likely serving a role in localized translation to ensure efficient phage propagation.https://doi.org/10.1371/journal.ppat.1012936
spellingShingle Wichanan Wannasrichan
Sucheewin Krobthong
Chase J Morgan
Emily G Armbruster
Milan Gerovac
Yodying Yingchutrakul
Patompon Wongtrakoongate
Jörg Vogel
Chanat Aonbangkhen
Poochit Nonejuie
Joe Pogliano
Vorrapon Chaikeeratisak
A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
PLoS Pathogens
title A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
title_full A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
title_fullStr A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
title_full_unstemmed A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
title_short A ribosome-interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation.
title_sort ribosome interacting jumbophage protein associates with the phage nucleus to facilitate efficient propagation
url https://doi.org/10.1371/journal.ppat.1012936
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