Bacteriophage-mediated competition in Bordetella bacteria - PubMed (original) (raw)

Bacteriophage-mediated competition in Bordetella bacteria

Jaewook Joo et al. Proc Biol Sci. 2006.

Abstract

Apparent competition between species is believed to be one of the principal driving forces that structure ecological communities, although the precise mechanisms have yet to be characterized. Here we develop a model system that isolates phage-mediated interactions by neutralizing resource competition with a large excess of nutrients, and consists of two genetically identical Bordetella strains that differ only in that one is the carrier of phage and the other is susceptible to the phage. We observe and quantify the competitive advantage of the bacterial strain bearing the prophage in both invading and in resisting invasion by the bacterial strain sensitive to the phage, and use our experimental measurements to develop a mathematical model of phage-mediated competition. The model predicts, and experimental evidence confirms, that the competitive advantage conferred by the lysogenic phage depends only on the phage pathology on the sensitive bacterial strain and is independent of other phage and host parameters, such as the infection-causing contact rate, the spontaneous and infection-induced lysis rates and the phage burst size. This work combines experimental and mathematical approaches to the study of phage-driven competition, and provides an experimentally tested framework for evaluation of the effects of pathogens/parasites on interspecific competition.

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Figures

Figure 1

Figure 1

Schematic of phage-mediated competition between two bacterial strains. The phage (Φ) is represented by a hexagon carrying a small thick line (Φ DNA). Bacteria are represented by a rectangle containing an inner circle (bacterial DNA), while the lysogens (Bb::Φ and BbGm::Φ) are represented by rectangles containing Φ DNA integrated into bacterial DNA. Gm indicates gentamicin resistance marker. All bacterial populations grow with identical growth rate r; lysogens are spontaneously lysed with a rate δ and have a net growth rate of r_−_δ. κ is the infection-causing contact rate, λ is the infection-induced lysis rate and P the pathogenicity of the phage.

Figure 2

Figure 2

The in vitro growth curves of B. bronchiseptica strains. (a) The three B. bronchiseptica strains, Bb::Φ (open squares), BbGm (filled circles) and Bb (filled diamonds), grow exponentially when grown separately. The straight line corresponds to a doubling time of 77 min. (b) Bb and BbGm grow at the same rate when co-cultured. We fit the growth curves of the two bacterial strains by using the theoretical model of equation (2.1) in the absence of lysogens and phage. The error bars denote the standard deviation of the number of colony forming units (CFU) of each bacterial strain.

Figure 3

Figure 3

In vitro experiments (symbols) and numerical simulations (lines) of (a) the invasion of the strain (Bb::Φ) exogenously and endogenously carrying the lysogenic phage to the susceptible strain (BbGm) and (b) the protection of Bb::Φ against the invading BbGm. Symbols and lines represent Bb::Φ (open squares, thick solid line), BbGm::Φ (open circles, thin solid line) and the total BbGm (filled circles, long-dashed line), respectively. BbGm::Φ are newly resistant bacteria which initially belonged to the sensitive strain, yet later became resistant by incorporating the prophage into their genome. See the text for the parameter values used for simulations. The error bars denote the standard deviation of the number of colony forming units (CFU) of each bacterial strain.

Figure 4

Figure 4

Independence of the steady-state outcome of phage-mediated competition on the initial phage concentration. Main: in vitro competition experiments of Bb::Φ (open symbols connected by a solid line) and the Gm-marked strain (filled symbols, dotted lines) with exogenously added phage concentrations of 10 (filled circles), 104 (filled squares) and 105 (filled diamonds) PFU ml−1. Inset: numerical simulations of the competition of Bb::Φ (solid line) and the total BbGm with three different initial phage concentrations of 101 (long-dashed line), 104 (dashed line) and 105 (dot-dashed line) PFU ml−1. We used the same parameter values as in figure 3_a_. The error bars denote the standard deviation of the number of colony forming units (CFU) of each bacterial strain.

Figure 5

Figure 5

Dependence of phage-mediated competition on the phage pathology P is observed in in vitro experiments (symbols) and numerical simulations (lines). Presented are time-evolutions of (a) the co-cultured BbΔ_prn_Gm (filled circles, solid line) and Bb::ΦΔ_orf_5 (open squares, dashed line) in the presence of exogenously added mutant phage (ΦΔ_orf_5) and (b) the co-cultured Bb::Φ (open squares, solid line) and the Gm-marked strain (filled circles, dashed line) in the presence of exogenously added lytic phage (ΦΔ_cI_). The parameters used for the numerical simulations are the same as in figure 3_a_, except _κ_=0 (and thus P_=0) in figure 5_a, and _P_=1 for lytic phage and P_=0.98 for lysogenic phage in figure 5_b. The error bars denote the standard deviation of the number of the colony forming units (CFU) of each bacterial strain.

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