XRE transcription factors conserved in Caulobacter and φCbK modulate adhesin development and phage production.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 22 08 2023
accepted: 03 11 2023
revised: 30 11 2023
medline: 4 12 2023
pubmed: 17 11 2023
entrez: 16 11 2023
Statut: epublish

Résumé

The xenobiotic response element (XRE) family of transcription factors (TFs), which are commonly encoded by bacteria and bacteriophage, regulate diverse features of bacterial cell physiology and impact phage infection dynamics. Through a pangenome analysis of Caulobacter species isolated from soil and aquatic ecosystems, we uncovered an apparent radiation of a paralogous XRE TF gene cluster, several of which have established functions in the regulation of holdfast adhesin development and biofilm formation in C. crescentus. We further discovered related XRE TFs throughout the class Alphaproteobacteria and its phages, including the φCbK Caulophage, suggesting that members of this cluster impact host-phage interactions. Here we show that a closely related group of XRE transcription factors encoded by both C. crescentus and φCbK can physically interact and function to control the transcription of a common gene set, influencing processes including holdfast development and the production of φCbK virions. The φCbK-encoded XRE paralog, tgrL, is highly expressed at the earliest stages of infection and can directly inhibit transcription of host genes including hfiA, a potent holdfast inhibitor, and gafYZ, an activator of prophage-like gene transfer agents (GTAs). XRE proteins encoded from the C. crescentus chromosome also directly repress gafYZ transcription, revealing a functionally redundant set of host regulators that may protect against spurious production of GTA particles and inadvertent cell lysis. Deleting the C. crescentus XRE transcription factors reduced φCbK burst size, while overexpressing these host genes or φCbK tgrL rescued this burst defect. We conclude that this XRE TF gene cluster, shared by C. crescentus and φCbK, plays an important role in adhesion regulation under phage-free conditions, and influences host-phage dynamics during infection.

Identifiants

pubmed: 37972151
doi: 10.1371/journal.pgen.1011048
pii: PGENETICS-D-23-00944
pmc: PMC10688885
doi:

Substances chimiques

Transcription Factors 0
Xenobiotics 0
Adhesins, Bacterial 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011048

Subventions

Organisme : NIGMS NIH HHS
ID : F32 GM141017
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131762
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

Copyright: © 2023 McLaughlin 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.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Maeve McLaughlin (M)

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America.

Aretha Fiebig (A)

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America.

Sean Crosson (S)

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America.

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Classifications MeSH