Diversity of Pseudomonas aeruginosa Temperate Phages

Abstract

Modern sequencing technologies have provided insight into the genetic diversity of numerous species, including the human pathogen Pseudomonas aeruginosa. Bacterial genomes often harbor bacteriophage genomes (prophages), which can account for upwards of 20% of the genome. Prior studies have found P. aeruginosa prophages that contribute to their host's pathogenicity and fitness. These advantages come in many different forms, including the production of toxins, promotion of biofilm formation, and displacement of other P. aeruginosa strains. While several different genera and species of P. aeruginosa prophages have been studied, there has not been a comprehensive study of the overall diversity of P. aeruginosa-infecting prophages. Here, we present the results of just such an analysis. A total of 6,852 high-confidence prophages were identified from 5,383 P. aeruginosa genomes from strains isolated from the human body and other environments. In total, 3,201 unique prophage sequences were identified. While 53.1% of these prophage sequences displayed sequence similarity to publicly available phage genomes, novel and highly mosaic prophages were discovered. Among these prophages, there is extensive diversity, including diversity within the functionally conserved integrase and C repressor coding regions, two genes responsible for prophage entering and persisting through the lysogenic life cycle. Analysis of integrase, C repressor, and terminase coding regions revealed extensive reassortment among P. aeruginosa prophages. This catalog of P. aeruginosa prophages provides a resource for future studies into the evolution of the species. IMPORTANCE Prophages play a critical role in the evolution of their host species and can also contribute to the virulence and fitness of pathogenic species. Here, we conducted a comprehensive investigation of prophage sequences from 5,383 publicly available Pseudomonas aeruginosa genomes from human as well as environmental isolates. We identified a diverse population of prophages, including tailed phages, inoviruses, and microviruses; 46.9% of the prophage sequences found share no significant sequence similarity with characterized phages, representing a vast array of novel P. aeruginosa-infecting phages. Our investigation into these prophages found substantial evidence of reassortment. In producing this, the first catalog of P. aeruginosa prophages, we uncovered both novel prophages as well as genetic content that have yet to be explored.

Keywords: Pseudomonas aeruginosa; prophages; temperate phages.

FIG 1

Network of P. aeruginosa predicted prophages. Prophages are the nodes color-coded by taxonomy: Inoviridae, Microviridae, Myoviridae, Podoviridae, Siphoviridae, or unknown. Prophages are connected by the number of shared genes between each prophage. Five separate connected components (CC) represent these prophages, labeled CC1 through CC5.

FIG 2

Phylogenetic tree of all annotated integrase coding regions.

FIG 3

Phylogenetic tree of all annotated C repressor coding regions.

FIG 4

Prophage membership shared between integrase clusters and terminase clusters. The largest terminase clusters tend to share the most prophages with the largest integrase clusters.

FIG 5

Prophage membership shared between C repressor clusters and terminase clusters. The largest terminase clusters tend to share the most prophages with the largest C repressor clusters.