The Photorhabdus genomic atlas: horizontal gene transfer, genome plasticity, and functional divergence characterize Photorhabdus evolutionary landscape

The genus Photorhabdus comprises a diverse group of bacteria with a dual lifestyle as insect pathogens and symbionts of entomopathogenic nematodes, yet the genomic mechanisms underpinning their diversification remain incompletely understood. Here, I performed a comprehensive comparative genomic analysis of 32 Photorhabdus taxa representing the full phylogenetic diversity of the genus to elucidate the evolutionary forces shaping its diversification. Phylogenomic reconstruction based on 1,888 core genes resolved the genus into six well-supported clades consistent with current taxonomy. Pangenome analysis revealed a large and highly diverse repertoire (10,364 gene clusters), dominated by rare and lineage-specific genes (~ 62%), despite a highly conserved genomic backbone. Functional enrichment analyses indicated that early diverged lineages are enriched in biosynthetic and homeostatic processes, particularly lipid metabolism and metal ion transport, whereas more recently diverged taxa show greater diversification in carbohydrate utilization, redox metabolism, and cell envelope functions. Biosynthetic gene cluster analysis uncovered a conserved core of secondary metabolite pathways alongside extensive, largely uncharacterized diversity, highlighting substantial untapped biosynthetic potential. The putative resistome is primarily structured by conserved multidrug efflux systems, complemented by sporadically distributed resistance determinants. Putative virulence-associated genes exhibit a similar pattern, with conserved regulatory and structural components but variable accessory factors that may contribute to differences in host-associated traits. Core metabolic pathways are highly conserved across the genus, whereas plasmids encode predominantly niche-associated and interaction-related functions. Extensive horizontal gene transfer, including potential contributions from bacterial, archaeal, eukaryotic, and viral sources, may have contributed to genome diversification, with predicted horizontally acquired genes enriched in functions associated with nutrient utilization, membrane remodeling, and secondary metabolism. Large-scale chromosomal rearrangements further highlight the structural plasticity of Photorhabdus genomes. Together, the findings of this study support a model in which a conserved genomic core is complemented by a highly dynamic accessory genome that may contribute to ecological specialization, host-associated adaptation, and metabolic diversification. This work provides a comprehensive framework for understanding Photorhabdus evolution and underscores its potential as a reservoir of novel bioactive compounds.