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Phage-encoded small RNA hijacks host replication machinery to support the phage lytic cycle

ABSTRACT: Bacteriophages (phages) significantly influence bacterial populations in their natural environment. However, one aspect that has not been thoroughly explored in the context of phage-bacteria interactions is the post-transcriptional regulation of gene expression, despite the growing attention it has received for bacterial physiology over the last two decades. Important players in this process are small RNAs (sRNAs) that regulate target mRNAs via base-pairing, typically using RNA chaperones like Hfq to facilitate this regulation. Here, we apply RIL-seq, to map in-vivo the sRNA-RNA network in Escherichia coli upon lambda phage infection. We highlight changes in the bacterial transcriptome and sRNA interactome while uncovering a novel phage-encoded sRNA that regulates key genes in E. coli. We decipher the molecular mechanism of the sRNA-mediated regulation and illustrate how it hijacks the host replication machinery and helps the infection cycle. Overall, we uncover an RNA-level regulatory layer that shapes the E. coli - lambda interactions.

ORGANISM(S): Escherichia coli str. K-12 substr. MG1655

PROVIDER: GSE279505 | GEO | 2025/12/18

REPOSITORIES: GEO

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Phage-encoded small RNA hijacks host replication machinery to support the phage lytic cycle

Project description:Bacteriophages (phages) significantly influence bacterial populations in their natural environment. However, one aspect that has not been thoroughly explored in the context of phage-bacteria interactions is the post-transcriptional regulation of gene expression, despite the growing attention it has received for bacterial physiology over the last two decades. Important players in this process are small RNAs (sRNAs) that regulate target mRNAs via base-pairing, typically using RNA chaperones like Hfq to facilitate this regulation. Here, we apply RIL-seq, to map in-vivo the sRNA-RNA network in Escherichia coli upon lambda phage infection. We highlight changes in the bacterial transcriptome and sRNA interactome while uncovering a novel phage-encoded sRNA that regulates key genes in E. coli. We decipher the molecular mechanism of the sRNA-mediated regulation and illustrate how it hijacks the host replication machinery and helps the infection cycle. Overall, we uncover an RNA-level regulatory layer that shapes the E. coli - lambda interactions.

2025-12-18 | GSE298101 | GEO

Phage-phage competition and biofilms affect interactions between two virulent bacteriophages and Pseudomonas aeruginosa

Project description:Virulent bacteriophages (or phages) are viruses that specifically infect and lyse a bacterial host. When multiple phages co-infect a bacterial host, the extent of lysis, dynamics of bacteria-phage and phage-phage interactions are expected to vary. The objective of this study is to identify the factors influencing the interaction of two virulent phages with different Pseudomonas aeruginosa growth states (planktonic, an infected epithelial cell line, and biofilm) by measuring the bacterial time-kill and individual phage replication kinetics. A single administration of phages effectively reduced P. aeruginosa viability in planktonic conditions and infected human lung cell cultures, but phage-resistant variants subsequently emerged. In static biofilms, the phage combination displayed initial inhibition of biofilm dispersal, but sustained control was achieved only by combining phages and meropenem antibiotic. In contrast, adherent biofilms showed tolerance to phage and/or meropenem, suggesting a spatiotemporal variation in the phage-bacterial interaction. The kinetics of adsorption of each phage to P. aeruginosa during single- or co-administration were comparable. However, the phage with the shorter lysis time depleted bacterial resources early and selected a specific nucleotide polymorphism that conferred a competitive disadvantage and cross-resistance to the second phage. The extent and strength of this phage-phage competition and genetic loci conferring phage resistance, are, however, P. aeruginosa genotype dependent. Nevertheless, adding phages sequentially resulted in their unimpeded replication with no significant increase in bacterial host lysis. These results highlight the interrelatedness of phage-phage competition, phage resistance and specific bacterial growth state (planktonic/biofilm) in shaping the interplay among P. aeruginosa and virulent phages.

2024-07-17 | GSE271537 | GEO

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

Project description:Bacteriophages are highly abundant viruses of bacteria. The major role of phages in shaping bacterial communities and their emerging medical potential as antibacterial agents has trig-gered a rebirth of phage research. To understand the molecular mechanisms by which phages hijack their host, omics technologies can provide novel insights into the organization of tran-scriptional and translational events occurring during the infection process. In this study, we ap-ply transcriptomics and proteomics to characterize the temporal patterns of transcription and protein synthesis during T4 phage infection of E. coli. 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. Moreover, the correlation of the phage transcriptome and proteome reveals specific T4 phage mRNAs and proteins that are temporally decoupled, suggesting post-transcriptional and translational regulation mechanisms. This study provides the first comprehensive insights into the molecular takeover of E. coli by bacteriophage T4. This data set represents a valuable resource for future studies seeking to study molecular and regulatory events during infection. We created a user-friendly online tool, POTATO4, available to the scientific community to access gene expression patterns for E. coli and T4 genes.

2022-11-09 | GSE211026 | GEO

Influence of the aminoglycoside antibiotic apramycin on host and phage DNA transcription during infection of S. venezuelae ATCC 10712 with phage Alderaan

Project description:Bacterial populations face the constant threat of viral predation exerted by bacteriophages (or phages). In response, bacteria have evolved a wide range of defense mechanisms against phage challenges. Here, we show that aminoglycosides, a well-known class of antibiotics produced by Streptomyces, are potent inhibitors of phage infection. We observed a broad phage inhibition by aminoglycosides. We demonstrate that aminoglycosides do not prevent the injection of phage DNA into bacterial cells but instead block an early step of the viral life cycle. In this context, we used RNA sequencing of S. venezuelae cells infected with phage Alderaan to comparatively investigate the influence of apramycin on phage DNA tanscription at two different time points after inital infection.

2021-04-30 | GSE171784 | GEO

Whole transcriptome analysis of PBMCs stimulated with either a P. aeruginosa phage PNM lysate or with its bacterial host P. aeruginosa

Project description:The ability of bacteriophages to kill bacteria is well known, as is their potential use as alternatives to antibiotics. As such, bacteriophages reach high doses locally through infection of their bacterial host in the human body. In this study we assessed the gene expression profile, by means of whole transcriptome analysis, of peripheral blood mononuclear cells (PBMCs) derived from a healthy human donor and stimulated with a Pseudomonas aeruginosa phage PNM lysate, or P. aeruginosa strain 573. The PBMCs were stimulated for 20 h, followed by lysis of the cells and RNA extraction. In total, three stimulations were performed: control sample (i.e. not stimulated), P. aeruginosa phage PNM lysate and P. aeruginosa strain 573. Each stimulation was conducted in triplicate. The transcriptome analysis showed that the phage induce a clear immunological responses. Both pro- and anti-inflammatory genes were up-regulated in the PBMCs in the presence of the phage or its bacterial host. Our results indicate that bacteriophages might play a bigger role in the immune response then previously described and might have a broader effect than the clearing of bacterial infections alone, such as the suppression of the immune response to benefit their own survival.

2017-03-02 | GSE95573 | GEO

Cao2010 - Epigenetic state of lysogeny in phage lambda

Project description:References: 1. Xiaomei Zhu, Lan Yin, Leroy Hood, David Galas and Ping Ao, Efficiency, Robustness and Stochasticity of Gene Regulatory networks in Systems biology: Lambda switch as a working example, 2006. 2. Adam Arkin, John Ross and Harley H. McAdams, Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells, 1998, Genetics, 149: 1633-1648. 3. GenBank sequence: NC_001416 is the whole genome sequence of phage lambda.

2005-01-01 | MODEL1308080003 | BioModels

Comparative transcriptomics reveals a conserved Bacterial Adaptive Phage Response (BAPR) to viral predation

Project description:Intrinsic and acquired defenses against bacteriophages, including Restriction/Modification, CRISPR/Cas, and Toxin/Anti-toxin systems have been intensely studied, with profound scientific impacts. However, adaptive defenses against phage infection analogous to adaptive resistance to antimicrobials have yet to be described. To identify such mechanisms, we applied an RNAseq-based, comparative transcriptomics approach in different \textit{Pseudomonas aeruginosa} strains after independent infection by a set of divergent virulent bacteriophages. A common host-mediated adaptive stress response to phages was identified that includes the Pseudomonas Quinolone Signal, through which infected cells inform their neighbors of infection, and what may be a resistance mechanism that functions by reducing infection vigor. With host transcriptional machinery left intact, we also observe phage-mediated differential expression caused by phage-specific stresses and molecular mechanisms. These responses suggest the presence of a conserved Bacterial Adaptive Phage Response mechanism as a novel type of host defense mechanism, and which may explain transient forms of phage persistence.

2018-01-19 | GSE109338 | GEO

K5 capsule and lipopolysaccharide are important in resistance to T4 phage attack in probiotic E. coli strain Nissle 1917

Project description:Rapidly growing antibiotic resistance among gastrointestinal pathogens, and the ability of antibiotics to induce the virulence of these pathogens makes it increasingly difficult to rely on antibiotics to treat gastrointestinal infections. The probiotic E. coli strain Nissle 1917 (EcN) is the active component of the pharmaceutical preparation Mutaflor® and has been successfully used in the treatment of gastrointestinal disorders. Gut bacteriophages are dominant players in maintaining the microbial homeostasis in the gut, however, their interaction with incoming probiotic bacteria remains to be at conception. The presence of bacteriophages in the gut makes it inevitable for any probiotic bacteria to be phage resistant, in order to survive and successfully colonize the gut. This study addresses the phage resistance of EcN, specifically against lytic T4 phage infection. From various experiments we could show that i) EcN is resistant towards T4 phage infection, ii) EcN’s K5 polysaccharide capsule plays a crucial role in T4 phage resistance and iii) EcN’s lipopolysaccharide (LPS) inactivates T4 phages and notably, treatment with the antibiotic polymyxin B which neutralizes the LPS destroyed the phage inactivation ability of isolated LPS from EcN. Our results further indicate that N-acetylglucosamine at the distal end of O6 antigen in EcN’s LPS could be the interacting partner with T4 phages. From our findings, we have reported for the first time, the role of EcN’s K5 capsule and LPS in its defense against T4 phages. In addition, by inactivating the T4 phages, EcN also protects E. coli K-12 strains from phage infection in tri-culture experiments. The combination of the identified properties is not found in other tested commensal E. coli strains. Furthermore, our research highlights phage resistance as an additional safety feature of EcN, a clinically successful probiotic E. coli strain.

2019-08-27 | GSE135946 | GEO

The effects of a phage protein gp70.1 on Pseudomonas aerugonosa

Project description:The phage protein gp70.1 encoded by Pseudomonas aerugonosa phage PaP3 was toxic to both P. aerugonosa and E. coli, microarry analysis was used to investigate the effects of gp70.1 on P. aerugonosa with three periods of bacterial growth.

2016-10-01 | GSE77297 | GEO

Modulation of plant immunity and bacterial virulence by phage biocontrol

Project description:Bacteriophages are increasingly recognised as key players in modulating plant-microbe interactions, including their potential in the biocontrol of plant pathogenic bacteria. In this study, we investigated the tripartite interaction between, Arabidopsis thaliana, the bacterial plant pathogen Xanthomonas campestris pv. campestris (Xcc), and the lytic phage Seregon. Using meta-transcriptomic profiling, we characterized host and pathogen responses during infection and phage treatment. While a single phage treatment did not lead to the eradication of Xcc, treatment with phage Seregon significantly mitigated Xcc-induced disease symptoms, restoring leaf growth to levels comparable to the uninfected control within 14 days post-inoculation. Our data revealed that phage-mediated protection is associated with early bacterial recognition and suppression of jasmonate (JA)-related responses in the host. Analysis of nuclear localized reporter plant cell lines further confirmed a significant reduction in ROS levels in phage-treated plants. Concurrently, Xcc exhibited significant transcriptional downregulation of key virulence factors in the presence of the phage, including the genes encoding the type III secretion system, its associated effectors, and components involved in flagella biosynthesis. Remarkably, phage treatment did not lead to a significant increase in bacterial resistance to phage infection, which is in stark contrast to in vitro conditions. Taken together, this study provides first mechanistic insight into how phages can be harnessed to shape plant-pathogen interactions and highlights their potential role in enhancing plant resilience through targeted modulation of both host immunity and pathogen behaviour.

2025-04-17 | GSE294853 | GEO

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