Genomic diversification and tailocin-mediated competition in animal-associated Xenorhabdus bacteria

Biotic interactions, including competition among bacteria mediated by phage-derived weapons, can profoundly shape microbial genomes. We found that compared to genomes across domain Bacteria, genomes from the animal-associated Xenorhabdus genus contain among the highest proportions of phage-related genes, and variation among strains in their total number of protein-coding genes was largely predicted by variation in total number of non-cargo phage genes per genome. A universal yet highly variable Xenorhabdus phage-related locus encoded xenorhabdicin tailocins, a key weapon in bacterial competition. The xenorhabdicin tailocin locus ranged in length from 12 to 41 kilobases and varied markedly within species. Concomitant with this variation, xenorhabdicins produced by six strains of X. nematophila differed in killing profiles towards each other. Mutants from two X. nematophila strains whose tailocin tail fibre genes were deleted lost their killing ability, while complementation experiments restored or shifted killing profiles, demonstrating that the tailocin locus is responsible for intraspecific killing and the tail fibre gene its specificity. We demonstrated the ecological importance of xenorhabdicin diversity by significantly associating broad differences in intraspecific killing profiles of mitomycin-induced cell lysates from 37 regionally sympatric X. bovienii strains with genes within the tailocin locus. The diversity of these genes and their rearrangements within the locus challenges our understanding of tailocin mechanics. We propose that frequent coinfection of insect hosts by multiple Xenorhabdus strains promotes strong selection for within-host competitive dominance as well as opportunities for genomic rearrangements, making this genus a valuable resource for examining bacterial evolution in an ecological context.