Abstract
Many bacteriophage populations display heterogeneity in their adsorption characteristics; a portion of the phage population remains free in solution throughout adsorption experiments (residual fraction). This residual fraction generally constitutes a minority of phages that exhibit significantly slower adsorption kinetics than the main phage stock (main fraction). While this phenomenon is likely the result of evolutionary driving forces, the present study demonstrates that the residual fraction is not always the result of phenotypic variations within a single genotype, as is generally thought. Experiments with phage T4 showed that two subgroups with distinct adsorption traits that were passed on to their progeny could be isolated from the original phage stock. Sequencing of genes involved in adsorption revealed two point mutations in gene 37 of residual fraction isolates, which resulted in modifications to the long tail-fiber, the organelle of attachment and host cell recognition. Adsorption studies consistently showed that T4 phage stocks amplified from residual fraction isolates had significantly lower adsorption efficiencies than those amplified from main fractions. The conducted experiments provide convincing evidence that the observed heterogeneity in T4 adsorption behavior is the result of conserved mutations to the phage genome and is not exclusively the result of phenotypic variations within the population. While it is believed high mutation rates exist to hasten phage adaptation, this study shows that this bet hedging strategy can also, in the short term, inadvertently handicap the phage's adsorption capabilities to a given host under normal infection conditions, resulting in the residual fraction observed in adsorption experiments.
Highlights
Heterogeneity in the adsorption characteristics of a bacteriophage population has been widely reported since the first half of the 20th century
A recent study on strains of phage l with varying adsorption rates concluded that the residual fraction was not due to genotypic variation because characteristics of the residual phages were not passed on to their progeny [8]
The authors suggested that the existence of the residual fraction may have evolved as a form of diversified bet-hedging [21]
Summary
Heterogeneity in the adsorption characteristics of a bacteriophage population has been widely reported since the first half of the 20th century. Schlesinger [1], working with Escherichia coli phages, observed that a subset of the population had extremely slow adsorption kinetics or failed to adsorb at all. He called this group the residual fraction (summarized by Adams [1] and Delbruck [2]). Delbruck [2] confirmed these findings and ruled out the possibility of this fraction resulting from an equilibrium between phage and bacteria This heterogeneity, whereby a fraction of the phage population either adsorbs extremely slowly or not at all in liquid media, has been reported in diverse tailed phage species. Similar observations have been noted for Bacillus subtilis phage PBS Z [5], Lactobacillus casei phage PL-1 [6], the flagella-targeting Caulobacter crescentus phage QCbK [7], various strains of phage l [8], numerous T-series phages [9, 10] and even the mycoplasma virus L3 [11]
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