Abstract

We discovered a novel interaction between phage P22 and its host Salmonella Typhimurium LT2 that is characterized by a phage mediated and targeted derepression of the host dgo operon. Upon further investigation, this interaction was found to be instigated by an ORFan gene (designated pid for phage P22 encoded instigator of dgo expression) located on a previously unannotated moron locus in the late region of the P22 genome, and encoding an 86 amino acid protein of 9.3 kDa. Surprisingly, the Pid/dgo interaction was not observed during strict lytic or lysogenic proliferation of P22, and expression of pid was instead found to arise in cells that upon infection stably maintained an unintegrated phage chromosome that segregated asymmetrically upon subsequent cell divisions. Interestingly, among the emerging siblings, the feature of pid expression remained tightly linked to the cell inheriting this phage carrier state and became quenched in the other. As such, this study is the first to reveal molecular and genetic markers authenticating pseudolysogenic development, thereby exposing a novel mechanism, timing, and populational distribution in the realm of phage–host interactions.

Highlights

  • Due to billions of years of co-evolution and their overpowering abundance in the biosphere, viruses of bacteria have a profound impact on the conduct and ecology of their hosts [1,2]

  • We extend on the intricacy of phage – host interactions and provide both genetic and direct cell biological evidence for the existence of a dedicated pseudolysogenic state in the Salmonella Typhimurium – phage P22 model system

  • MudK mutagenesis of Salmonella Typhimurium LT2 reveals a clone that responds to infection by phage P22

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Summary

Introduction

Due to billions of years of co-evolution and their overpowering abundance in the biosphere, viruses of bacteria (i.e. bacteriophages or phages) have a profound impact on the conduct and ecology of their hosts [1,2]. In many ecological niches phage – host associations often appear to defy the classical bifurcation into strict lytic or lysogenic development, as a large number of reports indicate a lysogenyindependent but stable co-existence between phages and their hosts. These phenomena are often vaguely referred to as pseudolysogeny, and hypothesize the existence of stable ‘‘phage carrier’’ cells in which the incoming phage has temporarily refrained from lytic or lysogenic development [11]. Despite its ecological importance [11,14], no formal molecular evidence currently exists for the presence of such a state, let alone its possible impact on the physiology of the cell

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