Comparative genomics of Pantoea allii lineages and distribution of ecologically relevant traits

<i>Pantoea allii</i>, one of four <i>Pantoea</i> species known to cause onion centre rot, is infrequently isolated from onion compared to its closely related onion-pathogenic species in the same genus. To better understand the genomic diversity and genetic determinants of pathogenicity in this species, we analysed a collection of 38 <i>P</i>. <i>allii</i> strains isolated from 2 primary ecological niches, plants and rainwater, across North and South American and African continents using comparative genomics and phylogenetic approaches. Core-genome phylogeny, average nucleotide identity and gene presence-absence analyses revealed three genetically distinct lineages. All strains harboured conserved biosynthetic gene clusters (BGCs) for quorum sensing, carotenoid production, siderophores and thiopeptides. In contrast, two phosphonate BGCs, key determinants of onion pathogenicity, exhibited lineage-specific distributions. Onion-associated strains from lineages 1 and 2 carried the Halophos BGC responsible for onion tissue necrosis and also encoded the <i>alt</i> gene cluster that confers tolerance to thiosulfinates. Lineage 3 strains, isolated from both onion and rainwater, either lacked a phosphonate BGC entirely or possessed the HiVir phosphonate BGC. In addition, lineage 3 strains lacked the <i>alt</i> cluster altogether. The localization of these virulence genes in the genome varied, with Halophos integrated in the chromosome, HiVir encoded on the conserved Large <i>Pantoea</i> Plasmid, and <i>alt</i> located on small, variable plasmids (plasmid B). The type IV secretion system (T4SS) and type VI secretion system (T6SS) showed variable genomic architectures, with plasmid-borne T4SSs and two chromosomal T6SS loci differing in conservation and gene content. Additionally, conserved Pantailocin phage islands were detected in most genomes. Overall, this study reveals that while core metabolic and competitive traits are conserved across <i>P. allii</i>, virulence-associated loci display lineage-specific distribution, reflecting ecological differentiation and evolutionary plasticity within the species.