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Virus-Host Interactions Gets Lousy: P1vir Phage Development Upon Impaired RNA Global Regulation in E. coli Cells

ABSTRACT: Bacteriophage P1 is one of the most commonly studied phages in molecular biology, and P1vir, its virulent derivative, has been widely used in almost every biotechnological laboratory as a useful genetic tool. Phage development depends on many host proteins and the cellular physiological state. In many cases, metabolic control is assessed by efficient and energy-saving riboregulation, and one of the major cellular hub of the global RNA regulation is the Hfq protein. Despite the fact that this factor was discovered as host factor necessary for Qβ bacteriophage replication, the role of Hfq in phage biology has not been extensively studied. We have found that deletion of the hfq gene resulted in impaired development of P1vir, suggesting its important role, but not indispensability, in the phage biology. We demonstrate global changes in the host-virus transcriptome during the infection. We have found that at different times after infection of the wild type strain (10 and 20 min), numerous hosts genes have been downregulated. On the other hand, in the Δhfq mutant, relatively small number of genes has been downregulated. Furthermore, numerous viral genes have been downregulated in the Δhfq mutant, comparing to the wild-type cells. Our results demonstrate that deficiency in global RNA regulation severely affects phage P1vir development. Thus, observed impaired P1vir development can be explained by abolition of proper cell re-programming during infection and/or impaired phage gene expression. The Hfq protein, as a global RNA hub, occurs in Escherichia coli and its homologues are present in other bacteria and archeons. Therefore, we anticipate that our results put new light on Hfq as a global phage regulator.

ORGANISM(S): Escherichia coli

PROVIDER: GSE262812 | GEO | 2025/12/31

REPOSITORIES: GEO

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Project description:Bacteriophage infection of Lactococcus lactis strains used in the manufacture of fermented milk products is a major threat for the dairy industry. A greater understanding of the global molecular response of the bacterial host following phage infection has the potential to identify new targets for the design of phage control measures for biotechnological processes. In this study, we have used whole-genome oligonucleotide microarrays to gain insights into the genomic intelligence driving the instinctive response of L. lactis subsp. lactis IL1403 to the onset of a challenge with the lytic prolate-headed phage c2. Following phage adsorption, the bacterium differentially regulated the expression of 61 genes belonging to 14 functional categories, and mostly to cell envelope (12 genes), regulatory functions (11 genes), and carbohydrate metabolism (7 genes). The nature of the differentially regulated genes suggests the orchestration of a complex response involving induction of cell envelope stress proteins, D-alanylation of cell-wall lipoteichoic acids (LTAs), restoration of the proton motive force (PMF), and energy conservation. Increased D-alanylation of LTAs would act as an adsorption blocking mechanism, which we speculate may allow the survival of a small percent of the cell population when facing more realistic in vivo low titer-phage attacks. The modification of LTAs decoration in response to phage c2 adsorption also suggests these cell wall structures as possible primary receptors for this phage. Restoration of a physiological PMF is achieved by regulating the expression of genes affecting the two main components of the PMF, and serves to reverse a drastic depolarization of the host membrane caused by phage adsorption. Down-regulation of energy-consuming metabolic activities and a switch to anaerobic respiration helps the bacterium to save energy in order to sustain the PMF and the overall response to phage. We finally propose that the overall transcriptional response of L. lactis IL1403 to the phage stimuli is orchestrated by the concerted action of Phage Shock Proteins and of the bivalent transcriptional regulator SpxB following activation by the two-component system CesSR. To our knowledge, this represents the first detailed description in L. lactis, and probably in Gram-positive bacteria, of the molecular mechanisms involved in the host response to the membrane perturbation mediated by phage adsorption. Two-condition experiment: IL1403 vs. Bacteriophage c2-infected IL1403 cells. Biological replicates: 2 controls, 2 infected, independently grown and harvested. Two technical replicates per array.

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Virus-Host Interactions Gets Lousy: P1vir Phage Development Upon Impaired RNA Global Regulation in E. coli Cells

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