The evolutionary tale of tailocins in Pectobacterium show genus-wide homologous recombination and inversions of tail fiber genes

Due to their ability to kill closely related strains, phage tail-like bacteriocins, also called tailocins, play an important role in shaping bacterial communities. One such tailocin, called carotovoricin, is also known to be present in the Pectobacterium genus. However, little is known about its evolutionary dynamics and the scope of impact on species interactions in this genus. To investigate the diversity and evolution of carotovoricin, we performed a genus-wide, phylogenetically-structured pangenome study. This analysis inferred that the gene cluster responsible for carotovoricin biosynthesis is conserved across the genus and is located in the same gene neighborhood in all the species. Within the carotovoricin cluster, the tail fiber genes, which determine the host range specificity, exhibit high variability and discordance with the species phylogeny. We show evidence for an evolutionary mechanism involving recombination-mediated exchange of these tail fiber loci across the entire Pectobacterium genus, which complements the previously known mechanism for DNA sequence inversion to maintain tailocin polymorphism at the population level. In addition, the ability to exchange tail-fiber loci in a highly targeted and genus-wide manner could influence the community dynamics in nutrient rich environments such as infected plant tissues. In conclusion, the strong signal for carotovoricin retention and ability to exchange tail fibers indicates that it significantly contributes to the community interactions of the Pectobacterium phytopathogens. Significance StatementA widespread presence of tailocins among various gram-negative bacteria and maintenance of their tail fiber diversity underscore their role in inter-bacterial interactions. A tailocin is also found to be conserved in Pectobacterium, a pathogen causing soft rot. However, the mechanism maintaining the diversity of the tailocin tail fibers, which enable recognition of the target bacteria, is not yet completely understood. Here, we characterized the genomic diversity of this tailocin and discovered that the diversity is maintained through the exchange of the tail fiber locus DNA across the genus.