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Well-temperate phage: optimal bet-hedging against local environmental collapses.

ABSTRACT: Upon infection of their bacterial hosts temperate phages must chose between lysogenic and lytic developmental strategies. Here we apply the game-theoretic bet-hedging strategy introduced by Kelly to derive the optimal lysogenic fraction of the total population of phages as a function of frequency and intensity of environmental downturns affecting the lytic subpopulation. "Well-temperate" phage from our title is characterized by the best long-term population growth rate. We show that it is realized when the lysogenization frequency is approximately equal to the probability of lytic population collapse. We further predict the existence of sharp boundaries in system's environmental, ecological, and biophysical parameters separating the regions where this temperate strategy is optimal from those dominated by purely virulent or dormant (purely lysogenic) strategies. We show that the virulent strategy works best for phages with large diversity of hosts, and access to multiple independent environments reachable by diffusion. Conversely, progressively more temperate or even dormant strategies are favored in the environments, that are subject to frequent and severe temporal downturns.

SUBMITTER: Maslov S

PROVIDER: S-EPMC4451807 | biostudies-other | 2015

REPOSITORIES: biostudies-other

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Project description:BackgroundEnvironmentally growing pathogens present an increasing threat for human health, wildlife and food production. Treating the hosts with antibiotics or parasitic bacteriophages fail to eliminate diseases that grow also in the outside-host environment. However, bacteriophages could be utilized to suppress the pathogen population sizes in the outside-host environment in order to prevent disease outbreaks. Here, we introduce a novel epidemiological model to assess how the phage infections of the bacterial pathogens affect epidemiological dynamics of the environmentally growing pathogens. We assess whether the phage therapy in the outside-host environment could be utilized as a biological control method against these diseases. We also consider how phage-resistant competitors affect the outcome, a common problem in phage therapy. The models give predictions for the scenarios where the outside-host phage therapy will work and where it will fail to control the disease. Parameterization of the model is based on the fish columnaris disease that causes significant economic losses to aquaculture worldwide. However, the model is also suitable for other environmentally growing bacterial diseases.ResultsTransmission rates of the phage determine the success of infectious disease control, with high-transmission phage enabling the recovery of the host population that would in the absence of the phage go asymptotically extinct due to the disease. In the presence of outside-host bacterial competition between the pathogen and phage-resistant strain, the trade-off between the pathogen infectivity and the phage resistance determines phage therapy outcome from stable coexistence to local host extinction.ConclusionsWe propose that the success of phage therapy strongly depends on the underlying biology, such as the strength of trade-off between the pathogen infectivity and the phage-resistance, as well as on the rate that the phages infect the bacteria. Our results indicate that phage therapy can fail if there are phage-resistant bacteria and the trade-off between pathogen infectivity and phage resistance does not completely inhibit the pathogen infectivity. Also, the rate that the phages infect the bacteria should be sufficiently high for phage-therapy to succeed.

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Well-temperate phage: optimal bet-hedging against local environmental collapses.

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