Phenotypic Stochasticity Protects Lytic Bacteriophage Populations From Extinction During the Bacterial Stationary Phase

Abstract

It is generally thought that the adsorption rate of a bacteriophage correlates positively with fitness, but this view neglects that most phages rely only on exponentially growing bacteria for productive infections. Thus, phages must cope with the environmental stochasticity that is their hosts’ physiological state. If lysogeny is one alternative, it is unclear how strictly lytic phages can survive the host stationary phase. Three scenarios may explain their maintenance: (1) pseudolysogeny, (2) diversified or (3) conservative bet-hedging. In order to better understand how a strictly lytic phage survives the stationary phase of its host, and how phage adsorption rate impacts this survival, we challenged two strictly lytic phage λ, differing in their adsorption rates, with stationary phase Escherichia coli cells. Our results showed that, pseudolysogeny was not responsible for phage survival and that, contrary to our expectation, high adsorption rate was not more detrimental during stationary phase than low adsorption rate. Interestingly, this last observation was due to the presence of the “residual fraction” (phages exhibiting extremely low adsorption rates), protecting phage populations from extinction. Whether this cryptic phenotypic variation is an adaptation (diversified bet-hedging) or merely reflecting unavoidable defects during protein synthesis remains an open question.

Evidence That the Heterogeneity of a T4 Population Is the Result of Heritable Traits

“…For example, “slow adsorbers” are known to account for 2–3% of the population of phage T1 under certain conditions [3] , [4] . Similar observations have been noted for Bacillus subtilis phage PBS Z [5] , Lactobacillus casei phage PL-1 [6] , the flagella-targeting Caulobacter crescentus phage φCbK [7] , various strains of phage λ [8] , numerous T-series phages [9] , [10] and even the mycoplasma virus L3 [11] .…”

Relationship Between the Genome Packing in the Bacteriophage Capsid and the Kinetics of Dna Ejection

“…It has been shown that the population heterogeneity can improve the fitness. 77,78 For phage infection, several mechanisms have already been identified as a source of stochasticity: (i) the host expression of phage receptors that imposes the phage binding probability 79 : (ii) the variation of the lysis time related to holing protein expression and diffusion 80,81 ; (iii) the decision at a subcellular level between lysis and lysogeny. 82,83 Concerning the phages, DNA organisation inside the capsid is a new source of stochasticity in addition to the variability in adsorption rate (possibly due to variable folding of tail fiber proteins 81 ).…”

Tradeoffs in bacteriophage life histories

“…It has long been known that a small percentage of a phage population (the "residual fraction") has an abnormally low adsorption rate, possibly as a bet-hedging strategy to prevent extinction. 37 That phenotype is apparently stochastic and non-heritable, 37 but more subtle modifications to adsorption rate might allow phage subpopulations to respond (relatively) rapidly to changes in host abundance. This process could be driven by the sensing of environmental conditions, leading to real-time phenotypic changes (e.g., lysis inhibition), or by mutations in genes whose products are involved in adsorption.…”