Phage-inducible chromosomal islands are ubiquitous within the bacterial universe

Alfred Fillol-Salom,John Chen,Rezheen F Abdulrahman,Roser Martínez-Rubio,Robert Davies,José R Penadés

doi:10.1038/s41396-018-0156-3

Abstract

Phage-inducible chromosomal islands (PICIs) are a recently discovered family of pathogenicity islands that contribute substantively to horizontal gene transfer, host adaptation and virulence in Gram-positive cocci. Here we report that similar elements also occur widely in Gram-negative bacteria. As with the PICIs from Gram-positive cocci, their uniqueness is defined by a constellation of features: unique and specific attachment sites, exclusive PICI genes, a phage-dependent mechanism of induction, conserved replication origin organization, convergent mechanisms of phage interference, and specific packaging of PICI DNA into phage-like infectious particles, resulting in very high transfer frequencies. We suggest that the PICIs represent two or more distinct lineages, have spread widely throughout the bacterial world, and have diverged much more slowly than their host organisms or their prophage cousins. Overall, these findings represent the discovery of a universal class of mobile genetic elements.

Highlights

The Staphylococcus aureus pathogenicity islands (SaPIs) are a novel class of phage satellites that are intimately related to certain temperate phages, of whose life cycles they parasitize
Following the nomenclature proposed for the elements present in the GP bacteria, the individual phage-inducible chromosomal islands (PICIs) are designated with reference to their species – EcCIn or PmCIn would be used for PICIs of Escherichia coli or Pasteurella multocida, respectively, where “n” would be used for the specific PICI-containing strain
The putative PICIs described here have a number of features in common. (i) Occurrence: they are very common among GN bacteria, especially in members of the Enterobacteriaeae and Pastuerellaceae (Gammaproteobacteria) (Table S1). (ii) Exclusivity: the KEGG orthology analyses confirmed that the GN PICI-encoded genes are PICI specific, not being present in other families of mobile genetic elements (MGEs) (Tables S2-S4)

Summary

Introduction

The Staphylococcus aureus pathogenicity islands (SaPIs) are a novel class of phage satellites that are intimately related to certain temperate (helper) phages, of whose life cycles they parasitize. SaPI-like elements are not unique to staphylococci, and we have recently demonstrated that they are widespread in Gram-positive (GP) cocci [22] This new family of mobile genetic elements (MGEs), that we have called generically phage-inducible chromosomal islands (PICIs), has very well conserved features [9, 23]. Transcribed in the opposite direction, the PICIs encode an excision function (xis), and a replication module consisting of a primase homolog (pri) and a replication initiator (rep), which are sometimes fused, followed by a replication origin (ori) To these genes, and transcribed in the same direction, PICIs encode genes involved in phage interference, and sometimes, a terminase small subunit homolog (terS) which is responsible for the high efficiency of the SaPI packaging [7]. In the SaPIs, accessory genes (usually involved in virulence; [9]) can be found either at the 3′ end of the elements or between the int and stl genes (Fig. 1)

Methods

Results

Conclusion