Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors

Bacteria encode sophisticated anti-phage systems that are diverse and versatile and display high genetic mobility. How this variability and mobility occurs remains largely unknown. Here, we demonstrate that a widespread family of pathogenicity islands, the phage-inducible chromosomal islands (PICIs), carry an impressive arsenal of defense mechanisms, which can be disseminated intra- and inter-generically by helper phages. These defense systems provide broad immunity, blocking not only phage reproduction, but also plasmid and non-cognate PICI transfer. Our results demonstrate that phages can mobilize PICI-encoded immunity systems to use them against other mobile genetic elements, which compete with the phages for the same bacterial hosts. Therefore, despite the cost, mobilization of PICIs may be beneficial for phages, PICIs, and bacteria in nature. Our results suggest that PICIs are important players controlling horizontal gene transfer and that PICIs and phages establish mutualistic interactions that drive bacterial ecology and evolution. [Display omitted] •PICIs carry an impressive arsenal of defense systems•PICI-encoded defense systems confer resistance to various mobile genetic elements•These defense systems block horizontal gene transfer•Phages benefit from mobilizing PICIs to target competing mobile genetic elements Phage-inducible chromosomal islands (PICIs) are highly mobile genetic elements that not only provide a diversity of defense systems in gram-positive and gram-negative bacteria, but can also be induced by a helper phage to protect that helper phage and the bacterial host from competing phages and other mobile genetic elements. This reveals a complex mutualistic relationship between bacteria, PICIs, and their helper phages that may broadly affect horizontal gene transfer.