Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis

Abstract

Phage-inducible chromosomal islands (PICIs) are a widespread family of highly mobile genetic elements that disseminate virulence and toxin genes among bacterial populations. Since their life cycle involves induction by helper phages, they are important players in phage evolution and ecology. PICIs can interfere with the lifecycle of their helper phages at different stages resulting frequently in reduced phage production after infection of a PICI-containing strain. Since phage defense systems have been recently shown to be beneficial for the acquisition of exogenous DNA via horizontal gene transfer, we hypothesized that PICIs could provide a similar benefit to their hosts and tested the impact of PICIs in recipient strains on host cell viability, phage propagation and transfer of genetic material. Here we report an important role for PICIs in bacterial evolution by promoting the survival of phage-mediated transductants of chromosomal or plasmid DNA. The presence of PICIs generates favorable conditions for population diversification and the inheritance of genetic material being transferred, such as antibiotic resistance and virulence genes. Our results show that by interfering with phage reproduction, PICIs can protect the bacterial population from phage attack, increasing the overall survival of the bacterial population as well as the transduced cells. Moreover, our results also demonstrate that PICIs reduce the frequency of lysogenization after temperate phage infection, creating a more genetically diverse bacterial population with increased bet-hedging opportunities to adapt to new niches. In summary, our results identify a new role for the PICIs and highlight them as important drivers of bacterial evolution.

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

“…Antiphage systems are also frequently colocated with MGEs, consistent with the proposal that phage predation (and defenses against it) accelerates lateral gene transfer and thereby, influences bacterial evolution ( 40 – 43 ). Known phage satellites, like PICIs and PLEs, have been recently recognized as key elements of antiphage defense systems ( 12 , 13 , 44 , 45 ). Some of the marine phage satellites reported here encoded known phage defense and interference genes (including small subunit terminases, restriction–modification systems, phage transcriptional regulators, and Abi-like genes), suggesting that they too may contribute to phage defense within their planktonic cellular hosts.…”

“…Phage satellites can influence host-cell phage immunity ( 5 , 10 ), the frequency of host gene transduction ( 9 , 11 – 14 ), host-cell pathogenicity ( 4 , 8 , 14 , 15 ), and host-cell and helper phage genome evolution ( 13 , 16 ). While evidence suggests that some habitat and host diversity may exist among known phage satellites ( 6 , 12 , 15 – 17 ), they have been clearly demonstrated to date mainly in several gram-positive genera ( 17 ) and a few gram-negative bacterial orders (Enterobacterales, Pasteurellales, Vibrionales), most of which are pathogens ( 6 , 8 , 10 , 16 ).…”

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

“…Many antiphage systems are frequently co-located with mobile genetic elements reinforcing the idea that phage predation (and defenses against it) accelerate lateral gene transfer, and help to drive bacterial evolution (40)(41)(42)(43). Known phage satellites, like PICIs and PLEs, have recently been recognized as key elements of antiphage defense systems (12,13,44,45). Some of the marine phage satellites we report here encoded known phage defense and interference genes (including CRISPR-Cas, R-M, phage transcriptional regulators, and Abi-like genes), suggesting they too may confer diverse phage defense functionalities to their planktonic cellular hosts.…”

“…Some of the marine phage satellites we report here encoded known phage defense and interference genes (including CRISPR-Cas, R-M, phage transcriptional regulators, and Abi-like genes), suggesting they too may confer diverse phage defense functionalities to their planktonic cellular hosts. As is the case with other mobile genetic elements (13, 39, 41, 43), these previously unrecognized marine phage satellites likely also impact the evolutionary rates and genetic diversity of host cells and the bacteriophage partners that they parasitize.…”

“…Phage satellites can influence host cell phage immunity (10,14), the frequency of host gene transduction (9,11,(12)(13)(14), host cell pathogenicity (4,14,15), and host cell and helper phage genome evolution (13,16). While evidence suggests that some habitat and host diversity may exist among known phage satellites (6,12,(15)(16)(17)(18), they have been demonstrated to date only in Gram positive bacteria (18) and a few Enterobacteriaceae and Pastuerellaceae pathogens (6,8,10).…”