A Filamentous Bacteriophage Protein Inhibits Type IV Pili To Prevent Superinfection of Pseudomonas aeruginosa

Schmidt, Amelia K; Fitzpatrick, Alexa; Schwartzkopf, Caleb M; Faith, Dominick R; Jennings, Laura K.; Coluccio, Alison; Hunt, Devin; Michaels, Lia A.; Hargil, Aviv; Chen, Qingquan; Bollyky, Paul L.; Dorward, David W.; Wachter, Jenny; Rosa, Patricia A.; Maxwell, Karen L.; Secor, Patrick R.

doi:10.1128/mbio.02441-21

Cited by 54 publications

(54 citation statements)

References 61 publications

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“…In our case, we discovered that conditioned media from phage producers inhibits phage infection. While superinfection immunity due to intracellular phage proteins has been reported in many systems (sieB of Salmonella phage P22 and E. coli phage lambda 49 , pIII of E. coli phage M13 51 , PfsE of Pseudomonas phage Pf 50 ), to the best of our knowledge, this is the first example of extracellular release of a phage protein to modulate immunity against self. Although mechanistically dissimilar, it is reminiscent of immune evasion by respiratory syncytial virus mediated by its extracellular soluble G protein 78,79 , suggesting that yet another mammalian immune system feature may have a prokaryotic counterpart 80 .…”

Section: Discussionmentioning

confidence: 81%

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A synthetic communication system uncovers extracellular immunity that self-limits bacteriophage transmission

Pathania

Hopper

Pandi

et al. 2022

Preprint

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Intercellular communication enables coordinated action by cells of microbial communities and multicellular organisms, often mediated by molecular exchange of information. Inspired by their success, synthetic biologists have recently started implementing population-level controls in engineered organisms with the aim of expanding circuit size and complexity. Yet, realising the true potential of multicellular synthetic biology requires an expanded communication alphabet as well as quantitative models to predict complex behaviour. Towards that aim, here we repurpose the M13 bacteriophage machinery for cell-to-cell communication between Escherichia coli cells and characterise the signalling dynamics. The fitted quantitative model includes the growth burden of the communication machinery, the relationship between cellular growth phase and the secretion-infection kinetics, and concurrent antibiotic selection. Limitations of deterministic models are demonstrated, with stochastic effects playing a key role in reproducing the observed infection kinetics. Surprisingly, we discover that the M13 minor coat protein pIII is released into the medium to confer extracellular immunity to uninfected cells. In a simulated gut environment, this mechanism enables the phage to farm uninfected bacterial cells for the future, increasing the overall success of both M13 and E. coli. In addition to establishing a tool for intercellular communication, our work uncovers the mutualistic nature of a phage-bacterial relationship that has evolved over long-term coexistence.

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Section: Discussionmentioning

confidence: 81%

“…There are examples of superinfection inhibition where an intracellular bacteriophage protein does not allow new phage infections 49,50 . In fact, gIII expression from the M13 bacteriophage is known to prevent the entry of a new phage into its host 51,52 , a result that we were able to confirm (Fig.…”

Section: Resultsmentioning

confidence: 99%

A synthetic communication system uncovers extracellular immunity that self-limits bacteriophage transmission

Pathania

Hopper

Pandi

et al. 2022

Preprint

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“…Prophages often express genes that provide competitive advantages to their host, including genes involved in bacterial pathogenicity [ 74 , 75 , 76 ] or virulence factors [ 77 , 78 , 79 , 80 , 81 , 82 ]. Prophages also have various mechanisms to prevent infection by other phages [ 83 , 84 , 85 , 86 ]. However, the role of phages in the spread of ARGs remains controversial.…”

Section: Lytic and Lysogenic Phages Contribute To Amrmentioning

confidence: 99%

Bacteriophage and Bacterial Susceptibility, Resistance, and Tolerance to Antibiotics

et al. 2022

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Bacteriophages, viruses that infect and replicate within bacteria, impact bacterial responses to antibiotics in complex ways. Recent studies using lytic bacteriophages to treat bacterial infections (phage therapy) demonstrate that phages can promote susceptibility to chemical antibiotics and that phage/antibiotic synergy is possible. However, both lytic and lysogenic bacteriophages can contribute to antimicrobial resistance. In particular, some phages mediate the horizontal transfer of antibiotic resistance genes between bacteria via transduction and other mechanisms. In addition, chronic infection filamentous phages can promote antimicrobial tolerance, the ability of bacteria to persist in the face of antibiotics. In particular, filamentous phages serve as structural elements in bacterial biofilms and prevent the penetration of antibiotics. Over time, these contributions to antibiotic tolerance favor the selection of resistance clones. Here, we review recent insights into bacteriophage contributions to antibiotic susceptibility, resistance, and tolerance. We discuss the mechanisms involved in these effects and address their impact on bacterial fitness.

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“…We recently reported that bacteriophage vB_PaeP_CMS1 does not utilize type IV pili as a receptor during infection of Pseudomonas aeruginosa ( 1 ). Here, we announce the genome sequence of the vB_PaeP_CMS1 bacteriophage.…”

Section: Announcementmentioning

confidence: 99%

Complete Genome Sequence of the N4-like Pseudomonas aeruginosa Bacteriophage vB_PaeP_CMS1

Faith

Kinnersley

Schwartzkopf

et al. 2022

Microbiol Resour Announc

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vB_PaeP_CMS1 is a lytic bacteriophage that infects Pseudomonas aeruginosa . Whole-genome sequencing revealed that vB_PaeP_CMS1 has a linear double-stranded DNA (dsDNA) genome composed of 72,673 bp, with a GC content of 54.9%, that harbors 92 predicted open reading frames, with the greatest genome homology to members of the family Podoviridae , genus Litunavirus .

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A Filamentous Bacteriophage Protein Inhibits Type IV Pili To Prevent Superinfection of Pseudomonas aeruginosa

Abstract: Pf bacteriophage (phage) are filamentous viruses that infect Pseudomonas aeruginosa and enhance its virulence potential. Pf virions can lyse and kill P. aeruginosa through superinfection, which occurs when an already infected cell is infected by the same or similar phage.

Cited by 54 publications

References 61 publications

A synthetic communication system uncovers extracellular immunity that self-limits bacteriophage transmission

A synthetic communication system uncovers extracellular immunity that self-limits bacteriophage transmission

Bacteriophage and Bacterial Susceptibility, Resistance, and Tolerance to Antibiotics

Complete Genome Sequence of the N4-like Pseudomonas aeruginosa Bacteriophage vB_PaeP_CMS1

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