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Phage satellites are genetic elements that couple their life cycle to that of helper phages they parasitize, interfering with phage packaging through the production of small capsids, where only satellites are packaged. So far, in all analyzed systems, the satellite-sized capsids are composed of phage proteins. Here, we report that a family of phage-inducible chromosomal islands (PICIs), a type of satellites, encodes all the proteins required for both the production of small-sized capsids and the exclusive packaging of the PICIs into these capsids. Therefore, this new family, named capsid-forming PICIs (cf-PICIs), only requires phage tails to generate PICI particles. Remarkably, the representative cf-PICIs are produced with no cost from their helper phages, suggesting that the relationship between these elements is not parasitic. Finally, our phylogenomic studies indicate that cf-PICIs are present both in gram-positive and gram-negative bacteria and have evolved at least three times independently to spread in nature. [Display omitted] • Capsid-forming PICIs (cf-PICIs) represent a widespread family of phage satellites • cf-PICIs produce small capsids to exclusively package their own dsDNA • cf-PICIs only hijack phage tails to produce infective particles • There are at least three groups of cf-PICIs that have emerged independently Alqurainy et al. discovered a widespread family of phage satellites encoding all the proteins required to produce small capsids, where satellite genomes are exclusively packaged. Therefore, to produce infective particles, these satellites only parasitize phage tails. These findings represent a new type of interaction between satellites and helper phages. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Phage-inducible chromosomal islands (PICIs) represent a novel and universal class of mobile genetic elements, which have broad impact on bacterial virulence. In spite of their relevance, how the Gram-negative PICIs hijack the phage machinery for their own specific packaging and how they block phage reproduction remains to be determined. Using genetic and structural analyses, we solve the mystery here by showing that the Gram-negative PICIs encode a protein that simultaneously performs these processes. This protein, which we have named Rpp (for redirecting phage packaging), interacts with the phage terminase small subunit, forming a heterocomplex. This complex is unable to recognize the phage DNA, blocking phage packaging, but specifically binds to the PICI genome, promoting PICI packaging. Our studies reveal the mechanism of action that allows PICI dissemination in nature, introducing a new paradigm in the understanding of the biology of pathogenicity islands and therefore of bacterial pathogen evolution. • PICI Rpp protein promotes PICI transfer while blocking phage reproduction • Rpp forms a heterocomplex with helper phage TerS • Crystal structures of Rpp alone or complexed with TerS were determined • TerS complexed with Rpp switches specificity from the phage DNA to the PICI genome Fillol-Salom et al. report that Gram-negative PICIs employ the Rpp protein to block helper phage reproduction. Rpp binds to helper phage TerS, and the Rpp-TerS heterocomplex enables PICIs to hijack the phage machinery for their own packaging. These findings reveal a mechanism used by Gram-negative PICIs to spread in nature. [ABSTRACT FROM AUTHOR]