Population Dynamics of Phage and Bacteria in Spatially Structured Habitats Using Phage λ and Escherichia coli

Abstract

Bacteria living in physically structured habitats are exposed heterogeneously to both resources and different types of phages. While there have been numerous experimental approaches to examine spatially distributed bacteria exposed to phages, there is little theory to guide the design of these experiments, interpret their results, or expand the inferences drawn to a broader ecological and evolutionary context. Plaque formation provides a window into understanding phage-bacterium interactions in physically structured populations, including surfaces, semisolids, and biofilms. We develop models to address the plaque dynamics for a temperate phage and its virulent mutants. The models are compared with phage -Escherichia coli system to quantify their applicability. We found that temperate phages gave an increasing number of gradually smaller colonies as the distance increased from the plaque center. For low-lysogen frequency this resulted in plaques with most of the visible colonies at an intermediate distance between the center and periphery. Using spot inoculation, where phages in excess of bacteria were inoculated in a circular area, we measured the frequency and spatial distribution of lysogens. The spot morphology of cII-negative (cII ؊ ) and cIII ؊ mutants of phage displays concentric rings of high-density lysogenic colonies. The simplest of these ring morphologies was reproduced by including multiplicity of infection (MOI) sensitivity in lysis-lysogeny decisions, but its failure to explain the occasional observation of multiple rings in cIII ؊ mutant phages highlights unknown features of this phage. Our findings demonstrated advantages of temperate phages over virulent phages in exploiting limited resources in spatially distributed microbial populations. IMPORTANCEPhages are the most abundant organisms on earth, and yet little is known about how phages and bacterial hosts are influencing each other in density and evolution. Phages can be either virulent or temperate, a difference that is highlighted when a spatially structured bacterial population is infected. Phage is a temperate phage, with a capacity for dormancy that can be modified by single gene knockouts. The stochastic bias in the lysis-lysogeny decision's probability is reflected in plaque morphologies on bacterial lawns. We present a model for plaque morphology of both virulent and temperate phages, taking into account the underlying survival of bacterial microcolonies. It reproduces known plaque morphologies and speaks to advantages of temperate phages in a spatially structured environment. T he active biomass on earth is dominated by prokaryotes, which constitute about half the amount of the carbon stored in living organisms (1). Bacteria are widely exposed to phages, which in turn are the most numerous inhabitants of our biosphere (2, 3). Phages have developed a diversity of behaviors that support their survival (survival strategies), which continues to inform our understanding of evolution and gene editing (4-8). One classical phage type ...

Antibiofilm potential of purified environmental bacteriophage preparations against early stage Pseudomonas aeruginosa biofilms

“…It must be noted that high rates of adsorption may not necessarily lead to all bacteriophages completing their infection cycle. Mitarai et al (2016) reported that plaque morphology can be affected by the nutritional state of the host bacterial cell, and the number of bacteriophages that can infect them. This is important, as the nutritional and metabolic state of bacterial cells within biofilms will be different to those in planktonic culture, as well as differences existing between early stage and mature biofilm-dwelling cells.…”

How pirate phage interferes with helper phage: Comparison of the two distinct strategies

“…We use the Lotka-Volterra type ordinary differential equations to model the population dynamics of the system, which has been used to describe temperate phage and bacteria population dynamics [18,23,29,26]. To extend the model 80 to the pirate-helper phage system described in Fig.…”

“…For the well-mixed case, we use the Lotka-Volterra type equations. For the plaque simulation, we let bacteria grow locally while 70 let phage and nutrient diffuse, describing the system using a reaction-diffusion type model [19,26]. In both cases, we consider time scale of an overnight, where effect of the induction and the mutation are negligible.…”

Estimating Optimal Lysogenic Propensity for Viruses in Stressed Environments

“…A number of theoretical models [5], [10], [11], [12] have 22 been proposed to explain the observed experimental trends. Although these 23 models do provide a possible understanding of the system, they have their own 24 limitations. Avlund et al [10] provide a game-theoretical model to explain the 25 decision between lysogeny and lysis, the parameters for which are similar to 26 those used in the current work.…”

“…15, 2018; -shown by the red curve with an extremely small error area. Classically, en-172 vironments have been assumed to be good [11], [24], thus missing out on the 173 variation caused by changes in the values of the parameters in bad environments. 174 It is interesting to note that as the environment becomes worse for phages, the 175 lysogenic propensity at a given M oI decreases.…”