Lineage-restricted genomic islands drive rhizosphere niche specialization in Pseudomonas capeferrum

In the rhizosphere, plant growth-promoting rhizobacteria play a pivotal role in plant health by efficiently colonizing roots and enhancing growth through diverse direct and indirect mechanisms. Many of these beneficial traits are associated with genomic islands (GEIs) acquired via horizontal gene transfer, yet their contribution to rhizosphere fitness remains poorly understood. Here, we report the whole-genome sequencing and comprehensive analysis of Pseudomonas putida strain IsoF, a highly efficient root colonizer originally isolated from the tomato rhizosphere that induces systemic resistance in plants. Phylogenomic analysis reclassified IsoF within the P. capeferrum group and revealed an extensive repertoire of GEIs encoding candidate functions to rhizosphere adaptation and plant growth promotion. Notably, IsoF harbours a unique combination of three GEIs absent in closely related strains. Phenotypic characterization and rhizosphere persistence assays using defined deletion mutants demonstrated that these islands significantly contribute to IsoF fitness and competitiveness in the rhizosphere. Together, our findings establish GEIs as key determinants of ecological success in beneficial rhizobacteria and position IsoF as a promising candidate for sustainable biocontrol applications.