How repeated outbreaks drive the evolution of bacteriophage communication: Insights from a mathematical model

Abstract

Communication based on small signalling molecules is widespread among bacteria. Recently, such communication was also described in bacteriophages. Upon infection of a host cell, temperate phages of the Bacillus subtilis-infecting SPbeta group induce the secretion of a phage-encoded signalling peptide, which is used to inform the lysis-lysogeny decision in subsequent infections: the phages produce new virions and lyse their host cell when the signal concentration is low, but favour a latent infection strategy, lysogenising the host cell, when the signal concentration is high. Here, we present a mathematical model to study the ecological and evolutionary dynamics of such viral communication. We show that a communication strategy in which phages use the lytic cycle early in an outbreak (when susceptible host cells are abundant) but switch to the lysogenic cycle later (when susceptible cells become scarce) is favoured over a bet-hedging strategy in which cells are lysogenised with constant probability. However, such phage communication can evolve only if phage-bacteria populations are regularly perturbed away from their equilibrium state, so that acute outbreaks of phage infections in pools of susceptible cells continue to occur. Our model then predicts the selection of phages that switch infection strategy when half of the available susceptible cells have been infected.