Two Lineages of Pseudomonas aeruginosa Filamentous Phages: Structural Uniformity over Integration Preferences

Abstract

Pseudomonas aeruginosa filamentous (Pf) bacteriophages are important factors contributing to the pathogenicity of this opportunistic bacterium, including biofilm formation and suppression of bacterial phagocytosis by macrophages. In addition, the capacity of Pf phages to form liquid crystal structures and their high negative charge density make them potent sequesters of cationic antibacterial agents, such as aminoglycoside antibiotics or host antimicrobial peptides. Therefore, Pf phages have been proposed as a potential biomarker for risk of antibiotic resistance development. The majority of studies describing biological functions of Pf viruses have been performed with only three of them: Pf1, Pf4 and Pf5. However, our analysis revealed that Pf phages exist as two evolutionary lineages (I and II), characterized by substantially different structural/morphogenesis properties, despite sharing the same integration sites in the host chromosomes. All aforementioned model Pf phages are members of the lineage I. Hence, it is reasonable to speculate that their interactions with P. aeruginosa and impact on its pathogenicity may be not completely extrapolated to the lineage II members. Furthermore, in order to organize the present numerical nomenclature of Pf phages, we propose a more informative approach based on the insertion sites, i.e. Pf-tRNA-Gly, -Met, -Sec, -tmRNA and -DR (direct repeats), which are fully compatible with one of five types of tyrosine integrases/recombinases XerC/D carried by these viruses. Finally, we discuss possible evolutionary mechanisms behind this division and consequences from the perspective of virus-virus, virus-bacterium and virus-human interactions.

Tripartite interactions between filamentous Pf4 bacteriophage,Pseudomonas aeruginosa, and bacterivorous nematodes

“…In the environment, nematodes and other bacterivores such as phagocytic amoeba can impose high selective pressures on bacteria [59-61]. The ability of Pf phage to increase P. aeruginosa fitness against environmental bacterivores may help explain why Pf prophages are so widespread amongst diverse P. aeruginosa strains [3, 62, 63]. Further, the ability of Pf phage to increase bacterial fitness against bacterivores in the environment may translate to an enhanced ability of P. aeruginosa Pf lysogens to exploit opportunities to infect susceptible vertebrate hosts, such as people with medical implants, diabetic ulcers, or cystic fibrosis.…”

“…In the environment, nematodes and other bacterivores such as phagocytic amoeba can impose high selective pressures on bacteria [59][60][61]. The ability of Pf phage to increase P. aeruginosa fitness against environmental bacterivores may help explain why Pf prophages are so widespread amongst diverse P. aeruginosa strains [3,62,63].…”

Pf Bacteriophage Inhibits Neutrophil Migration in the Lung

“…We and others have previously investigated the impact of Pf phages on their bacterial and human hosts. Pf is a genus of filamentous bacteriophages that infect the common bacterial pathogen P. aeruginosa and includes the phages Pf1-Pf8 (Knezevic et al, 2015;Mai-Prochnow et al, 2015;Hay and Lithgow, 2019;Fiedoruk et al, 2020). Pf phages are Inoviruses and have a single stranded .…”

“…We and others have previously investigated the impact of Pf phages on their bacterial and human hosts. Pf is a genus of filamentous bacteriophages that infect the common bacterial pathogen P. aeruginosa and includes the phages Pf1-Pf8 ( Knezevic et al, 2015; Mai-Prochnow et al, 2015; Hay and Lithgow , 2019; Fiedoruk et al, 2020). Pf phages are Inoviruses and have a single stranded (ss) DNA genome packaged within a helical filamentous structure made up of thousands of copies of the major coat protein CoaB ( Marvin et al, 2014; Hay and Lithgow , 2019; Roux et al, 2019).…”

Highlight—Evolution on the Outskirts: Virtual Issue on Viral Evolution

“…Another field of study involves understanding the effects that viruses have on their host organisms. Fiedoruk et al. (2020) performed an analysis of the filamentous bacteriophages of Pseudomonas aeruginosa , which are known to contribute to the bacterium’s pathogenicity by promoting biofilm formation, suppressing phagocytosis by macrophages, and sequestering cationic antibacterial compounds.…”