Coexistence of phage and bacteria on the boundary of self-organized refuges

Abstract

Bacteriophage are voracious predators of bacteria and a major determinant in shaping bacterial life strategies. Many phage species are virulent, meaning that infection leads to certain death of the host and immediate release of a large batch of phage progeny. Despite this apparent voraciousness, bacteria have stably coexisted with virulent phages for eons. Here, using individual-based stochastic spatial models, we study the conditions for achieving coexistence on the edge between two habitats, one of which is a bacterial refuge with conditions hostile to phage whereas the other is phage friendly. We show how bacterial density-dependent, or quorum-sensing, mechanisms such as the formation of biofilm can produce such refuges and edges in a self-organized manner. Coexistence on these edges exhibits the following properties, all of which are observed in real phage–bacteria ecosystems but difficult to achieve together in nonspatial ecosystem models: ( i ) highly efficient virulent phage with relatively long lifetimes, high infection rates and large burst sizes; ( ii ) large, stable, and high-density populations of phage and bacteria; ( iii ) a fast turnover of both phage and bacteria; and ( iv ) stability over evolutionary timescales despite imbalances in the rates of phage vs. bacterial evolution.

Spatial Structure Mitigates Fitness Costs in Host-Parasite Coevolution

“…We adapt the bacterium-phage model proposed by Heilmann et al (2010) to incorporate the GFG framework outlined above, thus allowing the evolution of varying degrees of generalism. We conduct simulations on a square grid of side length N p 100, where boundary effects are removed by wrapping the grid around the surface of a torus, so that all grid sites have exactly four orthogonal neighbors.…”

“…However, the role of local interactions on range expansion has yet to be determined. Here, we attempt to address this gap in the literature by adapting an individual-based model of bacteria and phages first proposed by Heilmann et al (2010). Although the model was originally used to explore the evolution of virulence in spatially structured populations, it can be readily adapted to serve our focus on range expansion by incorporating the multilocus GFG framework of Sasaki (2000).…”

“…Similarly, theoretical studies have generally been limited to metapopulation analyses (Frank 1993;Gandon et al 1996Gandon et al , 2008Damgaard 1999), which incorporate a certain degree of spatial structure but do not capture local interactions between individuals within subpopulations, which are known to be critical in many epidemiological scenarios (Rand et al 1995;Rhodes and Anderson 1996;Keeling et al 2001;Eames and Keeling 2002). Individual-based models are able to capture local interactions and have been used to study a diverse set of biological phenomena including the evolution of life histories and virulence (Boots and Sasaki 1999;Haraguchi and Sasaki 2000;Read and Keeling 2003;Heilmann et al 2010), altruism (Jansen and van Baalen 2006), and various other aspects of coevolution (Hartvigsen and Levin 1997; Kerr et al 2006;Mitchell et al 2006;Best et al 2011;Haerter et al 2011;Zaman et al 2011;Heilmann et al 2012). However, the role of local interactions on range expansion has yet to be determined.…”

Phage and bacteria support mutual diversity in a narrowing staircase of coexistence

“…Because of the extreme maximal growth rate of phages, the modeled ecology can exhibit a dramatic dynamic response to addition of strains, and transient oscillations can drive some strains to population levels equivalent to extinction. However, these extinctions may not represent real ecosystem behavior, as they would be softened by both the heterogeneity between individuals and spatial heterogeneity (Kerr et al, 2002;Haerter and Sneppen, 2012;Heilman et al, 2012). We therefore simplified our analysis to focus on the composition and evolution of sustainable ecosystems, defined as systems with coexistence steady states.…”

Phage selection for bacterial cheats leads to population decline

“…An increase in siderophore production may have both direct and indirect effects: it can favour growth through higher access to iron and/or regulate other potentially beneficial traits such as biofilm formation (e.g. [53]). Second, quorum sensing has been shown to influence phagebacteria interactions [54], and an increased activation of this system in the presence of phage may lead to the upregulation of public goods production and of pyoverdin in particular (e.g.…”