RNA-Sequencing Reveals the Progression of Phage-Host Interactions between φR1-37 and Yersinia enterocolitica

Abstract

Despite the expanding interest in bacterial viruses (bacteriophages), insights into the intracellular development of bacteriophage and its impact on bacterial physiology are still scarce. Here we investigate during lytic infection the whole-genome transcription of the giant phage vB_YecM_φR1-37 (φR1-37) and its host, the gastroenteritis causing bacterium Yersinia enterocolitica. RNA sequencing reveals that the gene expression of φR1-37 does not follow a pattern typical observed in other lytic bacteriophages, as only selected genes could be classified as typically early, middle or late genes. The majority of the genes appear to be expressed constitutively throughout infection. Additionally, our study demonstrates that transcription occurs mainly from the positive strand, while the negative strand encodes only genes with low to medium expression levels. Interestingly, we also detected the presence of antisense RNA species, as well as one non-coding intragenic RNA species. Gene expression in the phage-infected cell is characterized by the broad replacement of host transcripts with phage transcripts. However, the host response in the late phase of infection was also characterized by up-regulation of several specific bacterial gene products known to be involved in stress response and membrane stability, including the Cpx pathway regulators, ATP-binding cassette (ABC) transporters, phage- and cold-shock proteins.

Transcriptomic and Metabolomics Profiling of Phage–Host Interactions between Phage PaP1 and Pseudomonas aeruginosa

“…This pattern of bacterial response is similar to other phage–host studies (Lavigne et al, 2013; Leskinen et al, 2016; Zhao et al, 2016b) in which many host genes are repressed. Only a few DEGs (51, Supplementary Table S2) were upregulated, including membrane proteins involved in energy and small-molecule transport, such as narK1 , narH , narJ , and fptA .…”

“…A few studies have recently reported findings of phage–host interactions using transcriptomic and metabolomic approaches in P. aeruginosa , Yersinia enterocolitica, Bacillus subtilis , and the marine microbe Sulfitobacter sp. 2047 (Lavigne et al, 2013; Ankrah et al, 2014; Chevallereau et al, 2016; De Smet et al, 2016; Leskinen et al, 2016; Mojardin and Salas, 2016). Chevallereau et al (2016) used next-generation “omics” approaches to investigate the interactions between P. aeruginosa and bacteriophage PAK_P3 and found that RNA processing was hijacked by phage infection and that bacterial transcripts were significantly depleted.…”

Low-level predation by lytic phage phiIPLA-RODI promotes biofilm formation and triggers the stringent response in Staphylococcus aureus

“…Indeed, several recent studies have provided us with valuable information regarding gene expression of bacterial cells infected with lytic or lysogenic phages. Some examples are the articles about P. aeruginosa 89, Yersinia enterocolitica 48, E. coli 6 or L. lactis 57. However, we still had no information on S. aureus and, also importantly, none of these studies had attempted transcriptional profiling of surface-attached populations.…”

Identification of Essential Genes in the Salmonella Phage SPN3US Reveals Novel Insights into Giant Phage Head Structure and Assembly

“…One approach to understanding phage infections is to use omics approaches, including transcriptomics and metabolomics (26, 27); however, seeing a clear link between any individual phage gene and its functions is not always straightforward. Historically, the genetic system based on the T4 phage has been one of the most paradigm-shifting model systems in biology, and it is critical for our understanding of the fine structure of the gene and many of the founding principles of molecular genetics (28–31).…”