Phage mobility is a core determinant of phage–bacteria coexistence in biofilms

Abstract

Many bacteria are adapted for attaching to surfaces and for building complex communities, termed biofilms. The biofilm mode of life is predominant in bacterial ecology. So too is the exposure of bacteria to ubiquitous viral pathogens, termed bacteriophages. Although biofilm–phage encounters are likely to be common in nature, little is known about how phages might interact with biofilm-dwelling bacteria. It is also unclear how the ecological dynamics of phages and their hosts depend on the biological and physical properties of the biofilm environment. To make headway in this area, we develop a biofilm simulation framework that captures key mechanistic features of biofilm growth and phage infection. Using these simulations, we find that the equilibrium state of interaction between biofilms and phages is governed largely by nutrient availability to biofilms, infection likelihood per host encounter and the ability of phages to diffuse through biofilm populations. Interactions between the biofilm matrix and phage particles are thus likely to be of fundamental importance, controlling the extent to which bacteria and phages can coexist in natural contexts. Our results open avenues to new questions of host–parasite coevolution and horizontal gene transfer in spatially structured biofilm contexts.

Sustainability of spatially distributed bacteria-phage systems

“…For example, our diverging latency time with nutrient depletion means that the phages do not prey on stationary state bacteria, an assumption that is mostly correct but would fail for example for phage T7 preying on Escherichia coli 44 . Note that spatial structure is still relevant in such a case, as shown in protection by biofilm that hinders physical contact of phages to bacteria 30,32,55 . We use a relatively high decay rate for the phage, δ = 0.1 h −1 which is comparable to the larger values reported in the ocean 36 but significantly higher than what is reported in more stable media 26 .…”

“…It is worth noting that a similar approach of coupling mass-action growth and lattice model was taken in ref. 32 to simulate the phage attack on a biofilm with the spacial resolution of ~ 4 μm. We here consider length scales which are orders of magnitude larger where one lattice site can contain several of microcolonies.…”

Phage efficacy in infecting dual-strain biofilms ofPseudomonas aeruginosa

“…A recent study showed that Escherichia coli produces an amyloid fiber network that protects cells in a biofilm individually and reduces phage diffusion (41). Survival in the face of phage can instead occur because the bacteria reduce the expression of their phage receptors (42), or because they slow down growth as nutrients are depleted (40, 43, 44). Our data support a model whereby growth arrest can prevent phage infection (26, 32, 45–48).…”

Sustainability of spatially distributed bacteria-phage systems

“…in protection by biofilm that hinders physical contact of phages to bacteria [25,46]. Also 385 the equations do not consider temperate phages, which would only induce a collapse of 386 order 0.1 to 0.01 (typical recorded lysogeny frequencies [34]).…”