Abstract
Staphylococcus aureus pathogenicity islands (SaPIs) are phage satellites that exploit the life cycle of their helper phages for their own benefit. Most SaPIs are packaged by their helper phages using a headful (pac) packaging mechanism. These SaPIs interfere with pac phage reproduction through a variety of strategies, including the redirection of phage capsid assembly to form small capsids, a process that depends on the expression of the SaPI-encoded cpmA and cpmB genes. Another SaPI subfamily is induced and packaged by cos-type phages, and although these cos SaPIs also block the life cycle of their inducing phages, the basis for this mechanism of interference remains to be deciphered. Here we have identified and characterized one mechanism by which the SaPIs interfere with cos phage reproduction. This mechanism depends on a SaPI-encoded gene, ccm, which encodes a protein involved in the production of small isometric capsids, compared with the prolate helper phage capsids. As the Ccm and CpmAB proteins are completely unrelated in sequence, this strategy represents a fascinating example of convergent evolution. Moreover, this result also indicates that the production of SaPI-sized particles is a widespread strategy of phage interference conserved during SaPI evolution.This article is part of the themed issue ‘The new bacteriology’.
Highlights
The Staphylococcus aureus pathogenicity islands (SaPIs) are the prototypical members of a novel family of mobile genetic elements, the phage-inducible chromosomal islands (PICIs)
As mobile genetics elements show synteny, and as in pac SaPIs the genes involved in phage interference are located between the SaPI ori site and the virulence genes, we speculated that the cpm-like gene(s) would be located in a similar position in the SaPIbov5 genome
We have described packaging of a family of cos SaPIs by cos helper phages f12 and fSLT, and show that these SaPIs interfere with phage production by forming small capsids that are unable to package complete helper phage genomes
Summary
The Staphylococcus aureus pathogenicity islands (SaPIs) are the prototypical members of a novel family of mobile genetic elements, the phage-inducible chromosomal islands (PICIs). We recently identified a subfamily of SaPIs in which the complete operon I, except the 30 region of the SaPI terSSP gene, had been replaced by a DNA region, that we have termed ‘operon I-like’, containing a highly conserved phage cos site (electronic supplementary material, figure S1) and a set of conserved genes whose functions remain obscure (figure 1) These variants, represented by SaPIbov and SaPIbov5 [27], are induced by certain cos phages, such as f12 or fSLT, which all share basically the same cos site (electronic supplementary material, figure S1), and are efficiently packaged in infectious phage-like particles, leading to high-frequency intraand intergeneric transfer [9,28]. The models of the C-terminal portions of gp and Ccm were structurally aligned with MUSTANG [33] and this alignment was rendered with ESPRIPT v. 3.0 [34]
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