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XRE Transcription Factors in Caulobacter and φCbK Modulate Adhesion and Phage Viability [RNA-seq]

ABSTRACT: During infection, transcriptional changes in both the phage and its host bacterium influence the outcome of infection. The xenobiotic response element (XRE) family of transcription factors (TFs), which are commonly encoded by bacteria and phages, regulate diverse aspects of bacterial cell physiology and can impact phage infection dynamics. Through a pangenome analysis of Caulobacter species isolated from soil and aquatic ecosystems, we uncovered an apparent radiation of an 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 across the class Alphaproteobacteria and its phages, including the φCbK Caulophage, suggesting that members of this gene cluster impact host-phage interactions. Here we show that that a closely related group of XRE proteins, encoded by both C. crescentus and φCbK, can interact to form heteromeric associations and control the transcription of a common gene set, influencing processes such as adhesin development and the progression of φCbK infection. The φCbK XRE paralog, tgrL, is highly expressed at the earliest stages of infection and can directly repress transcription of hfiA, a potent adhesion factor, and gafYZ, a transcriptional activator of prophage-like gene transfer agents (GTAs) encoded on the C. crescentus chromosome. A group of C. crescentus XRE proteins 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 host XRE transcription factors reduced φCbK burst size, while overexpressing these genes or φCbK tgrL rescued this burst defect. We conclude that a large 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.

ORGANISM(S): Caulobacter vibrioides CB15

PROVIDER: GSE241056 | GEO | 2023/08/25

REPOSITORIES: GEO

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Project description:During infection, transcriptional changes in both the phage and its host bacterium influence the outcome of infection. The xenobiotic response element (XRE) family of transcription factors (TFs), which are commonly encoded by bacteria and phages, regulate diverse aspects of bacterial cell physiology and can impact phage infection dynamics. Through a pangenome analysis of Caulobacter species isolated from soil and aquatic ecosystems, we uncovered an apparent radiation of an 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 across the class Alphaproteobacteria and its phages, including the φCbK Caulophage, suggesting that members of this gene cluster impact host-phage interactions. Here we show that that a closely related group of XRE proteins, encoded by both C. crescentus and φCbK, can interact to form heteromeric associations and control the transcription of a common gene set, influencing processes such as adhesin development and the progression of φCbK infection. The φCbK XRE paralog, tgrL, is highly expressed at the earliest stages of infection and can directly repress transcription of hfiA, a potent adhesion factor, and gafYZ, a transcriptional activator of prophage-like gene transfer agents (GTAs) encoded on the C. crescentus chromosome. A group of C. crescentus XRE proteins 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 host XRE transcription factors reduced φCbK burst size, while overexpressing these genes or φCbK tgrL rescued this burst defect. We conclude that a large 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.

Project description:We used microarray analysis to investigate whole genome transcriptome dynamics of the marine cyanobacterium Prochlorococcus sp. strain MED4 and the T7-like podovirus P-SSP7 over a time course during the 8 hour latent period of lytic infection prior to cell lysis. Manuscript Summary: Interactions between bacterial hosts and their viruses (phages) lead to reciprocal genome evolution through a dynamic co-evolutionary process1-5. Phage-mediated transfer of host genes – often located in genome islands – has had a major impact on microbial evolution1, 4, 6. Furthermore, phage genomes have clearly been shaped by the acquisition of genes from their hosts2, 3, 5. Here we investigate whole-genome expression of a host and phage, the marine cyanobacterium Prochlorococcus and a T7-like cyanophage during lytic infection, to gain insight into these co-evolutionary processes. While most of the phage genome was linearly transcribed over the course of infection, 4 phage-encoded bacterial metabolism genes were part of the same expression cluster, even though they are physically separated on the genome. These genes — encoding photosystem II D1 (psbA), high-light inducible protein (hli), transaldolase (talC) and ribonucleotide reductase (nrd) — are transcribed together with phage DNA replication genes and appear to make up a functional unit involved in energy and deoxynucleotide production needed for phage replication in resource-poor oceans. Also unique to this system was the upregulation of numerous genes in the host during infection. These may be host stress response genes, and/or genes induced by the phage. Many of these host genes are located in genome islands and have homologues in cyanophage genomes. We hypothesize that phage have evolved to utilize upregulated host genes, leading to their stable incorporation into phage genomes and their subsequent transfer back to hosts in genome islands. Thus activation of host genes during infection may be directing the co-evolution of gene content in both host and phage genomes. Keywords: time course, viral infection, marine cyanobacteria, podovirus, bacteriophage, stress response

Project description:Cyanobacteria are highly abundant in the oceans where they are constantly exposed to lytic viruses. Some viruses are restricted to a narrow host range while others infect a broad range of hosts. It is currently unknown whether broad-host range phages employ the same infection program, or regulate their program in a host-specific manner to accommodate for the different genetic makeup and defense systems of each host. Here we used a combination of microarray and RNA-seq analyses to investigate the interaction of three phylogentically distinct Synechococcus strains, WH7803, WH8102, and WH8109, with the broad-host range T4-like myovirus, Syn9, during infection. Strikingly, we found that the phage led a nearly identical expression program in the three hosts despite considerable differences in host gene content. On the other hand, host responses to infection involved mainly host-specific genes, suggesting variable attempts at defense against infection. A large number of responsive host genes were located in hypervariable genomic islands, substantiating genomic islands as a major axis of phage-bacteria interactions in cyanobacteria. Furthermore, transcriptome analyses and experimental determination of the complete phage promoter map revealed three temporally regulated modules and not two as previously thought for cyanophages. In contrast to T4, an extensive, previously unknown regulatory motif drives expression of early genes and host-like promoters drive middle-gene expression. These promoters are highly conserved among cyanophages and host-like middle promoters extend to other T4-like phages, indicating that the well-known mode of regulation in T4 is not the rule among the broad family of T4-like phages. We investigated the infection process and transcriptional program of the P-TIM40 cyanophage during infection of a Prochlorococcus NATL2A host. The results are discussed in conjunction with results obtained from the infection process for the Syn9 cyanophage in three different Synechococcus hosts: WH7803 (Dufresne et al. 2008), WH8102 (Palenik et al. 2003) and WH8109 (sequenced as part of this study).

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XRE Transcription Factors in Caulobacter and φCbK Modulate Adhesion and Phage Viability [RNA-seq]

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