Lytic/Lysogenic Transition as a Life-History Switch

Abstract

The transition between lytic and lysogenic life cycles is the most important feature of the life-history of temperate viruses. To explain this transition, an optimal life-history model is offered based a discrete-time formulation of phage/bacteria population dynamics that features infection of bacteria by Poisson sampling of virions from the environment. The time step is the viral latency period. In this model, density-dependent viral absorption onto the bacterial surface produces virus/bacteria coexistence and density dependence in bacterial growth is not needed. The formula for the transition between lytic and lysogenic phases is termed the 'fitness switch'. According to the model, the virus switches from lytic to lysogenic when its population grows faster as prophage than as virions produced by lysis of the infected cells, and conversely for the switch from lysogenic to lytic. A prophage that benefits the bacterium it infects automatically incurs lower fitness upon exiting the bacterial genome, resulting in its becoming locked into the bacterial genome in what is termed here as a 'prophage lock'. The fitness switch qualitatively predicts the ecogeographic rule that environmental enrichment leads to microbialization with a concomitant increase in lysogeny, fluctuating environmental conditions promote virus-mediated horizontal gene transfer, and prophage-containing bacteria can integrate into the microbiome of a eukaryotic host forming a functionally integrated tripartite holobiont. These predictions accord more with the 'Piggyback-the-Winner' hypothesis than with the 'Kill-the-Winner' hypothesis in virus ecology.

Keywords: bacteriophage; ecogeographic rules; fitness switch; holobiont; hologenome; horizontal gene transfer; kill-the-winner; life-history; lysogenic; lytic; mathematical model; microbialization; phage; piggyback-the-winner; population dynamics; prophage lock; tripartite holobiont; viral biogeography.

Figure 1.

Phage/bacteria life cycles. Left: life cycle for virulent phages and for the lytic phase of temperate phages. Bacteria in the bacterial source pool in the environment are infected by free virus particles (virions) from the viral source pool according Poisson sampling. The infected bacteria are the site of viral replication, leading to the release of new virions and the death of the infected cells. The uninfected bacteria replicate to produce more bacteria available for infection to begin the next time step. Right: life cycle for the lysogenic phase of temperate phages. The virus is represented as a helix that is incorporated as a prophage into the genome of its bacterial host. The virus life cycle is coincident with the bacterial life cycle. The time step is the viral latency period.

Figure 2.

vs. , in brown, for density-dependent absorption from Equation (8). The diagonal line, in blue, indicates . The intersection of the brown curve with the blue line indicates an equilibrium point where virus and bacteria coexist provided the equilibrium is stable. Here, , , , and varies left to right from 2 to 20 in steps of 2.

Figure 3.

Left: Equilibrium viral ratio, as a function of . Right: Curve is eigenvalue evaluated at as a function of and line at marks the boundary between stable and unstable equilibria. The equilibria for below 14 are stable and characterized by a damped oscillatory approach, whereas the equilibria for above 14 are unstable. Here, , , , and varies from 1 to 20.

Figure 4.

Left: Trajectory of showing damped oscillation during approach to equilibrium. Right: Trajectory of showing approach to exponential bacterial population growth. Here, , , , , , and t_max =16.

Figure 5.

Infection discount. Here, , , and varies from 1 to 20.