The Staphylococcus aureus pathogenicity islands (SaPIs) are a cohesive family of extremely common chromosomal islands that contribute substantively to horizontal gene transfer, host adaptation and virulence (Novick et al., 2010). SaPIs are closely related to certain S. aureus temperate (helper) bacteriophages, whose life cycle they parasitise using different and complementary strategies representing a hallmark of molecular piracy (Ram et al., 2012; Ram et al., 2014). They represent a unique class of mobile genetic elements, the phage-inducible chromosomal islands (PICIs) with well-defined characteristics: unique and specific attachment sites, SOS-insensitive repressors, unique replication origin organization, and specific packaging of SaPI DNA into phage-like infectious particles resulting in very high transfer frequencies, which they enhance by interfering with helper phage reproduction (Penadés & Christie., 2015).
As the SaPIs represent a highly successful biological strategy, we assumed that similar elements would be widespread. On the basis of resemblance to the paradigmatic SaPI genome, we have readily identified large cohesive families of similar elements in the lactococci and pneumococci/streptococci plus a few such elements in Enterococcus faecalis.
Based on extensive ortholog analyses, we have found that the PICI elements in the four different genera represent distinct but parallel lineages, suggesting convergent evolution towards a highly successful life-style. Remarkably, we have characterised in depth the enterococcal element, EfCIV583, and have shown that it very closely resembles the SaPIs in functionality as well as in genome organization, setting the stage for expansion of the study of elements of this type. In summary, our findings greatly broaden the PICI family to include elements from at least three genera of cocci and represent the discovery of novel agents for horizontal dissemination of virulence and other important accessory genes among bacteria.