Independent Co-Option of a Tailed Bacteriophage into a Killing Complex in
            <i>Pseudomonas</i>

Hockett, Kevin L.; Renner, Tanya; Baltrus, David A.

doi:10.1128/mbio.00452-15

Cited by 75 publications

(134 citation statements)

References 87 publications

(115 reference statements)

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“…More recently, R-tailocins similar to those produced by P. aeruginosa have been identified in plant-associated Pseudomonas strains (11,16,17,23,24), suggesting that R-tailocin production may be an important competitive determinant of bacterial interactions for Pseudomonas inhabiting diverse environments, such as the plant microbiome. In the present study, we focused on Pseudomonas chlororaphis 30-84, a rhizosphere-colonizing strain selected for its ability to suppress take-all disease of wheat, caused by the fungal plant pathogen Gaeumannomyces graminis var.…”

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confidence: 99%

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Pseudomonas chlororaphis Produces Two Distinct R-Tailocins That Contribute to Bacterial Competition in Biofilms and on Roots

Dorosky

Pierson

et al. 2017

Appl Environ Microbiol

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R-type tailocins are high-molecular-weight bacteriocins that resemble bacteriophage tails and are encoded within the genomes of many Pseudomonas species. In this study, analysis of the P. chlororaphis 30-84 R-tailocin gene cluster revealed that it contains the structural components to produce two R-tailocins of different ancestral origins. Two distinct R-tailocin populations differing in length were observed in UV-induced lysates of P. chlororaphis 30-84 via transmission electron microscopy. Mutants defective in the production of one or both R-tailocins demonstrated that the killing spectrum of each tailocin is limited to Pseudomonas species. The spectra of pseudomonads killed by the two R-tailocins differed, although a few Pseudomonas species were either killed by or insusceptible to both tailocins. Tailocin release was disrupted by deletion of the holin gene within the tailocin gene cluster, demonstrating that the lysis cassette is required for the release of both R-tailocins. The loss of functional tailocin production reduced the ability of P. chlororaphis 30-84 to compete with an R-tailocin-sensitive strain within biofilms and rhizosphere communities. Our study demonstrates that Pseudomonas species can produce more than one functional R-tailocin particle sharing the same lysis cassette but differing in their killing spectra. This study provides evidence for the role of R-tailocins as determinants of bacterial competition among plant-associated Pseudomonas in biofilms and the rhizosphere.IMPORTANCE Recent studies have identified R-tailocin gene clusters potentially encoding more than one R-tailocin within the genomes of plant-associated Pseudomonas but have not demonstrated that more than one particle is produced or the ecological significance of the production of multiple R-tailocins. This study demonstrates for the first time that Pseudomonas strains can produce two distinct R-tailocins with different killing spectra, both of which contribute to bacterial competition between rhizosphere-associated bacteria. These results provide new insight into the previously uncharacterized role of R-tailocin production by plant-associated Pseudomonas species in bacterial population dynamics within surface-attached biofilms and on roots.KEYWORDS R-tailocin, bacterial competition, rhizosphere, Pseudomonas, bacteriocins, microbial ecology, rhizosphere-inhabiting microbes B acteria produce a diversity of bacteriocins to kill closely related competitors (1). Tailocins are high-molecular-weight (HMW) bacteriocins produced by a variety of bacteria that resemble bacteriophage tails (2-5). Tailocin particles are protease resistant, thermolabile, and sedimentable by ultracentrifugation (2). These particles have been studied extensively for the opportunistic human pathogen Pseudomonas aeruginosa, strains of which are capable of producing either or both R-type and F-type

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confidence: 99%

“…Producing strains are typically resistant to the R-tailocin they release (3,(16)(17)(18)(19). Although host-killing ranges of some strains have been characterized, the extent to which R-tailocins contribute to the competitive dynamics of bacterial communities is less well understood.…”

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confidence: 99%

Pseudomonas chlororaphis Produces Two Distinct R-Tailocins That Contribute to Bacterial Competition in Biofilms and on Roots

Dorosky

Pierson

et al. 2017

Appl Environ Microbiol

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“…Bacterial genomes often contain a range of intact and remnant prophage elements (1)(2)(3), and ecologically important bacterial traits are believed to be phage-derived (e.g., phage-derived bacteriocins) (4). Phage-related sequences are observed more frequently in pathogenic than nonpathogenic strains (5), and prophage acquisition can be associated with changes in pathogen virulence (6,7).…”

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confidence: 99%

Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

Davies

James

Williams

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Temperate phages drive genomic diversification in bacterial pathogens. Phage-derived sequences are more common in pathogenic than nonpathogenic taxa and are associated with changes in pathogen virulence. High abundance and mobilization of temperate phages within hosts suggests that temperate phages could promote withinhost evolution of bacterial pathogens. However, their role in pathogen evolution has not been experimentally tested. We experimentally evolved replicate populations of Pseudomonas aeruginosa with or without a community of three temperate phages active in cystic fibrosis (CF) lung infections, including the transposable phage, ɸ4, which is closely related to phage D3112. Populations grew as freefloating biofilms in artificial sputum medium, mimicking sputum of CF lungs where P. aeruginosa is an important pathogen and undergoes evolutionary adaptation and diversification during chronic infection. Although bacterial populations adapted to the biofilm environment in both treatments, population genomic analysis revealed that phages altered both the trajectory and mode of evolution. Populations evolving with phages exhibited a greater degree of parallel evolution and faster selective sweeps than populations without phages. Phage ɸ4 integrated randomly into the bacterial chromosome, but integrations into motility-associated genes and regulators of quorum sensing systems essential for virulence were selected in parallel, strongly suggesting that these insertional inactivation mutations were adaptive. Temperate phages, and in particular transposable phages, are therefore likely to facilitate adaptive evolution of bacterial pathogens within hosts.Pseudomonas aeruginosa | cystic fibrosis | mobile genetic element | experimental evolution | bacteriophage C omparative genomics suggests that temperate phages play an important role in the evolution and genomic diversification of bacterial pathogens (1). Bacterial genomes often contain a range of intact and remnant prophage elements (1-3), and ecologically important bacterial traits are believed to be phage-derived (e.g., phage-derived bacteriocins) (4). Phage-related sequences are observed more frequently in pathogenic than nonpathogenic strains (5), and prophage acquisition can be associated with changes in pathogen virulence (6, 7). Prophages can directly contribute accessory gene functions (1, 8) or disrupt bacterial genes by insertional inactivation. Of particular note are the transposable class of temperate phages (also known as mutator phages), including D3112 of Pseudomonas aeruginosa (9, 10), which integrate throughout the chromosome disrupting existing genes and increasing the supply of mutations available to selection. Recent reports of high rates of phage mobilization within hosts (11) and high temperate phage abundance in humans (12), including at sites of chronic infection where phage particles have been observed to exceed bacterial host densities by 10-to 100-fold (13), suggests that temperate phages could play an important role in driving within-host...

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“…For example, R-type pyocins are related to PS17-like tails (51), RTBs of C. difficile are related to phiC2-like phages (21), and the Pseudomonas syringae RTB is related to a Mu-like tail structure (50). The same can be said for noncontractile PTLBs.…”

Section: Discussionmentioning

confidence: 93%

“…PTLBs appear to be widespread among the members of the bacterial kingdom, with examples from Rhizobium lupini (41), Xenorhabdus nematophilus (42), Xenorhabdus bovienii (43), Erwinia carotovora (44), Yersinia enterocolitica (45), Erwinia amylovora (46), Budvicia aquatic (47), Pragia fontium (47), Pseudomonas fluorescens (48), Stenotrophomonas maltophilia (49), Clostridium difficile (21), Pseudomonas aeruginosa (1), and Pseudomonas syringae (50). Those that have been studied in detail do not appear to share a single common PTLB ancestor, suggesting that each arose independently.…”

Section: Discussionmentioning

confidence: 99%

F-Type Bacteriocins of Listeria monocytogenes: a New Class of Phage Tail-Like Structures Reveals Broad Parallel Coevolution between Tailed Bacteriophages and High-Molecular-Weight Bacteriocins

et al. 2016

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Listeria monocytogenes is a significant foodborne human pathogen that can cause severe disease in certain high-risk individuals. L. monocytogenes is known to produce high-molecular-weight, phage tail-like bacteriocins, or "monocins," upon induction of the SOS system. In this work, we purified and characterized monocins and found them to be a new class of F-type bacteriocins. The L. monocytogenes monocin genetic locus was cloned and expressed in Bacillus subtilis, producing specifically targeted bactericidal particles. The receptor binding protein, which determines target cell specificity, was identified and engineered to change the bactericidal spectrum. Unlike the F-type pyocins of Pseudomonas aeruginosa, which are related to lambda-like phage tails, monocins are more closely related to TP901-1-like phage tails, structures not previously known to function as bacteriocins. Monocins therefore represent a new class of phage tail-like bacteriocins. It appears that multiple classes of phage tails and their related bacteriocins have coevolved separately in parallel. IMPORTANCEPhage tail-like bacteriocins (PTLBs) are structures widespread among the members of the bacterial kingdom that are evolutionarily related to the DNA delivery organelles of phages (tails). We identified and characterized "monocins" of Listeria monocytogenes and showed that they are related to the tail structures of TP901-1-like phages, structures not previously known to function as bacteriocins. Our results show that multiple types of envelope-penetrating machines have coevolved in parallel to function either for DNA delivery (phages) or as membrane-disrupting bacteriocins. While it has commonly been assumed that these structures were coopted from phages, we cannot rule out the opposite possibility, that ancient phages coopted complex bacteriocins from the cell, which then underwent adaptations to become efficient at translocating DNA.T wo types of high-molecular-mass (Ͼ10 6 -Da), phage tail-like bacteriocins (PTLBs), the R type and the F type, are known to exist in the bacterial kingdom (1, 2). R-type bacteriocins (RTBs) are contractile nanotube machines evolutionarily related to Myoviridae tails (e.g., that of bacteriophage T4) (3), type 6 secretion systems (4, 5), insecticidal protein injector complexes (6, 7), and structures involved in bacterium-marine animal interactions (8). RTBs are composed of a tube surrounded by a contractile sheath (9). At one end of the sheath is a complex baseplate structure to which six receptor binding proteins (RBPs) are attached. RTBs kill target bacteria by first binding to a receptor on the cell surface via RBPs. This event triggers sheath contraction, which then drives the tube structure through the cell envelope. The result is a dissipation of the membrane potential and cell death. Contact with a single RTB particle is sufficient to kill a cell (10). Far less studied are the F-type bacteriocins (FTBs). These high-molecular-weight bactericidal protein structures are evolutionarily related to the nonco...

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Independent Co-Option of a Tailed Bacteriophage into a Killing Complex in Pseudomonas

Cited by 75 publications

References 87 publications

Pseudomonas chlororaphis Produces Two Distinct R-Tailocins That Contribute to Bacterial Competition in Biofilms and on Roots

Pseudomonas chlororaphis Produces Two Distinct R-Tailocins That Contribute to Bacterial Competition in Biofilms and on Roots

Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

F-Type Bacteriocins of Listeria monocytogenes: a New Class of Phage Tail-Like Structures Reveals Broad Parallel Coevolution between Tailed Bacteriophages and High-Molecular-Weight Bacteriocins

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