Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors

Fillol-Salom, Alfred; Rostøl, Jakob T.; Ojiogu, Adaeze D.; Chen, John; Douce, Gill; Humphrey, Suzanne; Penadés, José R.

doi:10.1016/j.cell.2022.07.014

Cited by 56 publications

(58 citation statements)

References 71 publications

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“…They also often associate with WYL-domain containing proteins, transcriptional regulators that are enriched in phage defense islands (3,30,31). Furthermore, the genome neighborhood also encodes several viral proteins and integrases, in agreement with recent reports that mobile genetic elements (MGE) represent primary carriers of defense islands (14,26,32). These findings further support the involvement of the Shield systems in bacterial immunity.…”

Section: Shieldsupporting

confidence: 86%

“…Previous studies have demonstrated that bacterial defense systems cluster together in chromosomal hotspots, defined as ‘defense islands’ and that their mobilisation is dependent on mobile genetic elements (4, 25, 26). Genetic neighborhood analysis of known anti-phage systems has allowed the systematic discovery of many novel defense systems (10, 11, 13, 14).…”

Section: Resultsmentioning

confidence: 99%

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Shield co-opts an RmuC domain to mediate phage defence acrossPseudomonasspecies

Macdonald

Strahl

Blower

et al. 2022

Preprint

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Competitive bacteria-bacteriophage interactions have resulted in the evolution of a plethora of bacterial defense systems preventing phage propagation. In recent years, computational and bioinformatic approaches have underpinned the discovery of numerous novel bacterial defense systems. Anti-phage systems are frequently encoded together in genomic loci termed defense islands. Here we report the identification and characterisation of a novel anti-phage system, which we have termed Shield, that forms part of the Pseudomonas defensive arsenal. The Shield system comprises a membrane-bound protein, ShdA, harboring an RmuC domain. Heterologous production of ShdA alone is sufficient to mediate bacterial immunity against a panel of phages. We show that ShdA homologues can degrade phage DNA in vitro and, when expressed in a heterologous host, can alter the organisation of chromosomal DNA to a nucleoid structure. Further analysis reveals that Shield can be divided into four subtypes, three of which contain additional components that in some cases can modulate the activity of ShdA and/or provide additional lines of phage defence. Collectively, our results identify a new player within the Pseudomonas bacterial immunity arsenal that displays a novel mechanism of protection, and reveals a surprising role of RmuC domains in phage defence.

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Section: Shieldsupporting

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Shield co-opts an RmuC domain to mediate phage defence acrossPseudomonasspecies

Macdonald

Strahl

Blower

et al. 2022

Preprint

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“…The current explosion anti-phage immune systems discovered in bacterial genomes has prompted the analysis their genomic positioning. Fascinating examples of MGE transferred hotspots of anti-phage immunity have been documented that control ecological outcomes during phage-host interactions in Vibrio and E. coli, for example (7)(8)(9)(29)(30)(31). In contrast to these phage defense MGEs, however, here we show that core defense hotspots (cDHS) with conserved genomic markers flanking immunity regions can be predictive of an immune locus.…”

Section: Discussioncontrasting

confidence: 49%

Core Defense Hotspots withinPseudomonas aeruginosaare a consistent and rich source of anti-phage defense systems

Johnson

Laderman

Huiting

et al. 2022

Preprint

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Bacteria use a diverse arsenal of anti-phage immune systems, including CRISPR-Cas and restriction enzymes. Identifying the full defense repertoire of a given species is still challenging, however. Here, we developed a computational tool to broadly identify anti-phage systems, which was applied to >180,000 genomes available on NCBI, revealingPseudomonas aeruginosato possess the most diverse anti-phage arsenal of any species with >200 sequenced genomes. Using network analysis to identify the common neighbors of anti-phage systems, we surprisingly identified two highly conserved core defense hotspot loci (cDHS1 and cDHS2). Across more than 1,000 P. aeruginosa strains, cDHS1 is up to 224 kb (mean: 34 kb) with varied arrangements of at least 31 immune systems while cDHS2 has 24 distinct systems (mean: 15.4 kb). cDHS1/2 are present in mostP. aeruginosaisolates, in contrast to highly variable mobile DHSs. Most cDHS genes are of unknown function potentially representing new anti-phage systems, which we validated by identifying a novel anti-phage system (Shango) commonly encoded in cDHS1. Identification of core gene markers that flank immune islands could be a simple approach for immune system discovery and may represent popular landing spots for diverse MGEs carrying anti-phage systems.

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“…The Psu-Delta-Sid operon of P4-like phage satellites performs a unique and conserved helper subversion strategy; the capsid assembly and head-tail adaptor genes of cfPICI means that this is the only satellite known so far that hijacks only part of the helpers’ virions; and PLEs have evolved genetic machinery to not only subvert a specific incoming virulent phage, but also to kill its bacterial host upon excision. Interestingly, this strategy might also be used by some PICI, that were recently described to encode an abortive infection system (10), and P4-like satellites can also encode (less drastic) anti-phage defense systems (e.g. retrons) (9).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, individual bacterial genomes often carry satellites of different families, suggesting that competitive or antagonistic interactions between phage satellites of different families may occur. Together with the ubiquity of prophages, and the oft-present anti-phage defense systems in phage satellites (6, 9, 10), this highlights the complex networks that dictate the emergence and maintenance of these phage satellites and phages, as well as the fitness and survival of their bacterial hosts. Our results reinforce the idea that phage satellites play an important role in the microbial world.…”

Section: Discussionmentioning

confidence: 99%

Identification and characterization of thousands of bacteriophage satellites across bacteria

Sousa

Fillol-Salom

Penadés

et al. 2022

Preprint

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Bacteriophage-bacteria interactions are affected by phage satellites, elements that exploit phages for transfer between bacterial cells. Satellites can encode defense systems, antibiotic resistance genes, and virulence factors, but their number and diversity are unknown for lack of a tool to identify them. We developed a flexible and updateable program to identify satellites in bacterial genomes — SatelliteFinder — and use it to identify the best described families: P4-like, phage inducible chromosomal islands (PICI), capsid-forming PICI, and phage-inducible chromosomal island-like elements (PLE). We vastly expanded the number of described elements to ~5000, finding hundreds of bacterial genomes with two different families of satellites, and dozens of Escherichia coli genomes with three. Most satellites were found in Proteobacteria and Firmicutes, but some are in novel taxa such as Actinobacteria. We characterized the gene repertoires of satellites, which are variable in size and composition, and their genomic organization, which is very conserved. With the partial exception of PICI and cfPICI, there are few homologous core genes between families of satellites, and even fewer homologous to phages. Hence, phage satellites are ancient, diverse, and probably evolved multiple times independently. Occasionally, core genes of a given family of satellites are found in another, suggesting gene flow between different satellites. Given the many elements found in spite of our conservative approach, the many bacteria infected by phages that still lack known satellites, and the recent proposals for novel families, we speculate that we are at the beginning of the discovery of massive numbers and types of satellites. SatelliteFinder is accessible for the community as a Galaxy service at https://galaxy.pasteur.fr/root?tool_id=toolshed.pasteur.fr/repos/fmareuil/satellitefinder/SatelliteFinder/0.9

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Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors

Cited by 56 publications

References 71 publications

Shield co-opts an RmuC domain to mediate phage defence acrossPseudomonasspecies

Shield co-opts an RmuC domain to mediate phage defence acrossPseudomonasspecies

Core Defense Hotspots withinPseudomonas aeruginosaare a consistent and rich source of anti-phage defense systems

Identification and characterization of thousands of bacteriophage satellites across bacteria

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