Pangenomics to understand prophage dynamics in the Pectobacterium genus and the radiating lineages of Pectobacterium brasiliense

Bacterial pathogens of the genus <i>Pectobacterium</i> are responsible for soft-rot and blackleg diseases in a wide range of crops and have a global impact on food production. The emergence of new lineages and their competitive succession is frequently observed in <i>Pectobacterium</i> species, in particular in <i>Pectobacterium brasiliense</i>. With a focus on one such recently emerged <i>P. brasiliense</i> lineage in the Netherlands that causes blackleg in potatoes, we studied genome evolution in this genus using a reference-free graph-based pangenome approach. We clustered 1,977,865 proteins from 454 <i>Pectobacterium</i> spp<i>.</i> genomes into 30,156 homology groups. The <i>Pectobacterium</i> genus pangenome is open, and its growth is mainly contributed by the accessory genome. Bacteriophage genes were enriched in the accessory genome and contributed 16% of the pangenome. Blackleg-causing <i>P. brasiliense</i> isolates had increased genome size with high levels of prophage integration. To study the diversity and dynamics of these prophages across the pangenome, we developed an approach to trace prophages across genomes using pangenome homology group signatures. We identified lineage-specific as well as generalist bacteriophages infecting <i>Pectobacterium</i> species. Our results capture the ongoing dynamics of mobile genetic elements, even in the clonal lineages. The observed lineage-specific prophage dynamics provide mechanistic insights into <i>Pectobacterium</i> pangenome growth and contribution to the radiating lineages of <i>P. brasiliense</i>.