XRE transcription factors conserved in Caulobacter and φCbK modulate adhesin development and phage production
- PMID: 37972151
- PMCID: PMC10688885
- DOI: 10.1371/journal.pgen.1011048
XRE transcription factors conserved in Caulobacter and φCbK modulate adhesin development and phage production
Abstract
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.
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.
Conflict of interest statement
The authors have declared that no competing interests exist.
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Update of
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XRE Transcription Factors Conserved in Caulobacter and φCbK Modulate Adhesin Development and Phage Production.bioRxiv [Preprint]. 2023 Aug 20:2023.08.20.554034. doi: 10.1101/2023.08.20.554034. bioRxiv. 2023. Update in: PLoS Genet. 2023 Nov 16;19(11):e1011048. doi: 10.1371/journal.pgen.1011048. PMID: 37645952 Free PMC article. Updated. Preprint.
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