Superinfection exclusion factors drive a history-dependent switch from vertical to horizontal phage transmission

Temperate bacterial viruses are commonly thought to favor vertical (lysogenic) transmission over horizontal (lytic) transmission when the virion-to-host-cell ratio is high and available host cells become scarce. In P22-infected Salmonella Typhimurium populations, however, we find that host subpopulations become lytically consumed despite high phage-to-host ratios that would normally favor lysogeny. These subpopulations originate from the proliferation of P22-free siblings that spawn off from P22-carrier cells from which they cytoplasmically inherit P22-borne superinfection exclusion factors (SEFs). In fact, we demonstrate that the gradual dilution of these SEFs in the growing subpopulation of P22-free siblings restricts the number of incoming phages, thereby imposing the perception of a low phage-to-host ratio that favors lytic development. Although their role has so far been neglected, our data indicate that phage-borne SEFs can spur complex infection dynamics and a history-dependent switch from vertical to horizontal transmission in the face of host-cell scarcity.