Abstract
Monitoring the complex transmission dynamics of a bacterial virus (temperate phage P22) throughout a population of its host (Salmonella Typhimurium) at single cell resolution revealed the unexpected existence of a transiently immune subpopulation of host cells that emerged from peculiarities preceding the process of lysogenization. More specifically, an infection event ultimately leading to a lysogen first yielded a phage carrier cell harboring a polarly tethered P22 episome. Upon subsequent division, the daughter cell inheriting this episome became lysogenized by an integration event yielding a prophage, while the other daughter cell became P22-free. However, since the phage carrier cell was shown to overproduce immunity factors that are cytoplasmically inherited by the P22-free daughter cell and further passed down to its siblings, a transiently resistant subpopulation was generated that upon dilution of these immunity factors again became susceptible to P22 infection. The iterative emergence and infection of transiently resistant subpopulations suggests a new bet-hedging strategy by which viruses could manage to sustain both vertical and horizontal transmission routes throughout an infected population without compromising a stable co-existence with their host.
Highlights
Viruses that infect microorganisms are ubiquitous in nature and often outnumber their hosts by an order of magnitude [1]
Extensive co-evolution with their host has shaped bacterial viruses into the most abundant and sophisticated pathogens known to date
How these important viral pathogens manage to safely exploit their host without jeopardizing stable co-existence remains a central question, since horizontal transmission can reduce the number of susceptible host cells and cause pathogen extinction, while vertical transmission impairs pathogen abundance
Summary
Viruses that infect microorganisms are ubiquitous in nature and often outnumber their hosts by an order of magnitude [1] Their predatory behavior imposes a tremendous selective pressure able to affect host mutation rates [2], direct the global biogeochemical carbon flux [3] and structure microbial communities in many environments, including the gastrointestinal tract [3,4,5]. In case of temperate phages, the incoming phage chromosome can alternatively decide to lysogenize the host and persist as a dormant prophage that remains episomal or integrates in the host chromosome, where it becomes stably replicated and segregated, to ensure further vertical transmission [12,13] In this lysogenic state, the genes supporting lytic development are typically repressed, with production of the corresponding phage-encoded repressor often being sustained by a toggle switch mechanism [14]
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