Integrated genomic and metabolomic insights into sesame rhizosphere-derived multi-trait Pseudomonas aeruginosa SIRJ8 with salinity stress alleviation and biocontrol potential

Abstract

Abstract Plant growth-promoting rhizobacteria (PGPR) offer microbe-based models for understanding crop resilience under environmental stress; however, environmental bacteria exhibiting both plant-beneficial functions and opportunistic pathogenic traits remain poorly understood, complicating their safe translation into agricultural applications. To address this gap, the present study undertakes an integrated genomic-metabolomic analysis of Pseudomonas aeruginosa SIRJ8, a strain isolated from the sesame ( Sesamum indicum L.) rhizosphere. Functionally, P. aeruginosa SIRJ8 displayed robust plant growth promoting attributes and tolerance to salinity levels up to 7.5% NaCl under in vitro conditions. It also showed pronounced antagonistic activity, achieving up to 82.7% inhibition of Fusarium spp. mycelial growth and 54.9% reduction of post-harvest tomato rot specifically against F. fujikuroi . Furthermore, in planta experiments showed that SIRJ8 significantly improved rice (BRRI Dhan 28) growth relative to the corresponding uninoculated plants exposed to the same salinity level, increasing shoot length by 49.6% and dry biomass by 50.3% under 150 mM NaCl. Genomic analysis revealed a 6.59 Mb genome with an open pan-genome architecture (α = 0.11). Among 169 strain-specific genes, we identified determinates for nutrient acquisition ( pqqF , tonB2 ), salinity resilience ( kshB , cfa ), and biocontrol ( hcp , chitinase class I). Genome mining via antiSMASH identified 21 biosynthetic gene clusters, including 100% homologous pathways for hydrogen cyanide and pseudopaline alongside several uncharacterized NRPS-like and RiPP-like clusters, suggesting a diverse specialized metabolome for competition and iron acquisition. GC-MS profiling and molecular docking identified key metabolites, including diketopiperazines and phenolic compounds, as potent candidates for fungal growth inhibition. While SIRJ8 harbors several canonical virulence-associated determinants (type III and type VI secretion systems, toxA , exoS , exoT , exoY genes), phenotypic biosafety assays demonstrated non-hemolytic behaviour and antibiotic susceptibility profile characteristic of non-clinical, environmental isolates. Collectively, this work delivers high-resolution mechanistic insights into the genomic and metabolomic features of P. aeruginosa SIRJ8, highlighting the functional and ecological intricacy of rhizosphere-associated bacteria. Although SIRJ8 exhibited multiple plant-beneficial traits, its virulence-associated genomic repertoire precludes its consideration as an agricultural bioinoculant at present and underscores the necessity of comprehensive biosafety evaluation before any practical application.