A domesticated phage suppresses competitors in historical and modern metapopulations of pathogenic bacteria

Bacteria have repeatedly repurposed the machinery of their viruses (bacteriophage) to kill strains of neighboring bacteria. These bacteriophage (phage)-derived elements are strain-specific in their killing activity, and this specificity has been proposed to drive bacterial population dynamics. Direct evidence of the impact of phage-derived elements on natural populations over time is limited. Here we identified viral sequences in a metapopulation of wild plant-associated Pseudomonas spp. genomes. We discovered that the most abundant viral cluster does not encode an intact phage but instead encodes a tailocin: a phage-derived element that bacteria use to kill bacterial competitors. Each pathogenic Pseudomonas sp. strain carries one of a few distinct tailocin variants, which target variable polysaccharides in the outer membrane of co-occurring pathogenic strains. Analysis of historic herbarium samples from the past 170 years revealed that the same tailocin and receptor variants have persisted in the Pseudomonas populations for at least two centuries, suggesting the continued use of a defined set of tailocin haplotypes and receptors. These results indicate that tailocin genetic diversity can be mined to develop targeted "tailocin cocktails" for microbial control.

Methods
Phylogeny is from Karasov TL, Almario J, Friedemann C, Ding W, Giolai M, Heavens D, Kersten S, Lundberg DS, Neumann M, Regalado J, Neher RA, Kemen E, Weigel D. Arabidopsis thaliana and Pseudomonas Pathogens Exhibit Stable Associations over Evolutionary Timescales. Cell Host Microbe. 2018 Jul 11;24(1):168-179.e4. doi: 10.1016/j.chom.2018.06.011. PMID: 30001519; PMCID: PMC6054916.

Core genes were found using panX, and alignments of these core gene sets were generated with pal2nal.