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

Competition between microbes is widespread in nature, especially among those that are closely related. To combat competitors, bacteria have evolved numerous protein-based systems (bacteriocins) that kill strains closely related to the producer. In characterizing the bacteriocin complement and killing spectra for the model strain Pseudomonas syringae B728a, we discovered that its activity was not linked to any predicted bacteriocin but is derived from a prophage. Instead of encoding an active prophage, this region encodes a bacteriophage-derived bacteriocin, termed an R-type syringacin. This R-type syringacin is striking in its convergence with the well-studied R-type pyocin of P. aeruginosa in both genomic location and molecular function. Genomic alignment, amino acid percent sequence identity, and phylogenetic inference all support a scenario where the R-type syringacin has been co-opted independently of the R-type pyocin. Moreover, the presence of this region is conserved among several other Pseudomonas species and thus is likely important for intermicrobial interactions throughout this important genus.

Evolutionary innovation is often achieved through modification of complexes or processes for alternate purposes, termed co-option. Notable examples include the co-option of a structure functioning in locomotion (bacterial flagellum) to one functioning in protein secretion (type three secretion system). Similar co-options can occur independently in distinct lineages. We discovered a genomic region in the plant pathogen Pseudomonas syringae that consists of a fragment of a bacteriophage genome. The fragment encodes only the tail of the bacteriophage, which is lethal toward strains of this species. This structure is similar to a previously described structure produced by the related species Pseudomonas aeruginosa. The two structures, however, are not derived from the same evolutionary event. Thus, they represent independent bacteriophage co-options. The co-opted bacteriophage from P. syringae is found in the genomes of many other Pseudomonas species, suggesting ecological importance across this genus.