From kill the winner to eliminate the winner in open phage-bacteria systems

Abstract

Phages and bacteria manage to coexist and sustain ecosystems with a high diversity of strains, despite limited resources and heavy predation. This diversity can be explained by the “kill the winner” model where virulent phages predominantly prey on fast-growing bacteria and thereby suppress the competitive exclusion of slower-growing bacteria. Here we computationally investigate the robustness of these systems against invasions, where new phages or bacteria may interact with more than one of the resident strains. The resulting interaction networks were found to self-organize into a network with strongly interacting specialized predator-prey pairs, resembling that of the “kill the winner” model. Furthermore, the “kill the winner” dynamics is enforced with the occasional elimination of even the fastest-growing bacteria strains due to a phage infecting the fast and slow growers. The frequency of slower-growing strains was increased with the introduction of even a few non-diagonal interactions. Hence, phages capable of infecting multiple hosts play significant roles both in the evolution of the ecosystem by eliminating the winner and in supporting diversity by allowing slow growers to coexist with faster growers.

Author summary

We demonstrate that in an open system of phages and bacteria with very limited resources, a bacterial strain that has a high growth rate can still be outcompeted by a slower-growing strain if they have a common phage. The impact of this on ecosystem structure is significant as soon as there is a small probability to have a common phage among bacterial strains. Furthermore, by analysing the structure of the interaction network we show that it self-organizes into a network with strongly interacting specialized predator-prey pairs, in order to reduce phages competition. Nevertheless, the presence of the remaining links is very important for the network dynamics since even a few of them significantly enhance the frequency of slower-growing strains.