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Integrated omics reveal time-resolved insights into T4 phage infection of E. coli on proteome and transcriptome level

ABSTRACT: Bacteriophages are highly abundant viruses of bacteria. The major role of phages in microbial ecology to shape bacterial communities and their emerging medical potential as antibacterial agents have triggered a rebirth of phage research. It is of particular interest to understand the molecular mechanisms by which phages gain control over their host. Omics technologies such as next-generation sequencing and protein-profiling technologies can provide novel insights into transcriptional and translational events occurring during the infection process. Thereby, the temporal organization of the transcriptome and proteome of the phage and their bacterial hosts can be monitored. In this study, we performed next-generation sequencing and proteomics to study the transcriptome and proteome of the T4 phage and its host during the infection in a time-resolved manner. Our data shows the temporally resolved appearance of bacteriophage T4 transcripts and proteins, confirming previously described subgrouping of T4 gene products into early, middle and late infection phases. We observe specific early transcripts giving rise to middle or late proteins indicating the existence of previously not reported post-transcriptional regulatory mechanisms controlling the translation of T4 mRNAs. Moreover, we investigated the stability of E. coli-originated transcripts and proteins in the course of infection, identifying degradation of E. coli transcripts and preservation of the host proteome. This study provides the first comprehensive insights into the transcriptomic and proteomic takeover by the bacteriophage T4, exemplifying the power and value of high-throughput technologies to simultaneously characterize multiple gene expression events. Moreover, we created a user-friendly application available to the entire scientific community to access gene expression patterns for their host and phage genes of interest.

INSTRUMENT(S): Orbitrap Exploris 480

ORGANISM(S): Escherichia Coli

SUBMITTER: Timo Glatter

LAB HEAD: Timo Glatter

PROVIDER: PXD035873 | Pride | 2022-09-19

REPOSITORIES: Pride

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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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Integrated omics reveal time-resolved insights into T4 phage infection of E. coli on proteome and transcriptome level

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