Unusual concurrence of P-solubilizing and biocontrol traits under P-limitation in plant-beneficial Pseudomonas aeruginosa P4: insights from in vitro metabolic and gene expression analysis

Abstract

Plant-beneficial fluorescent Pseudomonas species with concurrent P-solubilizing and biocontrol traits could have improved rhizospheric survival and efficacy; this rare ability being subject to diverse environmental and endogenous regulations. This study correlates growth patterns, time-course analysis of selected metabolites, non-targeted metabolomics of exometabolites and selected gene expression analysis to elucidate P-limitation-induced physiological shifts enabling co-production of metabolites implied in P-solubilization and biocontrol by P. aeruginosa P4 (P4). P-limited culture supernatants showed enhanced production of selected biocontrol metabolites such as pyocyanin, pyoverdine and pyochelin and IAA while maintaining biomass yield despite reduced growth rate and glucose consumption. Non-targeted exometabolomics further indicated that P-limitation positively impacted pentose phosphate pathway as well as pyruvate, C5-branched dibasic acid and amino acid metabolism. Its correlation with unusually reduced aroC expression and growth phase-dependent changes in the expression of key biosynthetic genes pchA, pchE, pchG, pvdQ and phzM implied a probable regulation of biosynthesis of chorismate-derived secondary metabolites, not neglecting the possibility of multiple factors influencing the gene expression profiles. Similar increase in biocontrol metabolite production was also observed in Artificial Root Exudates (ARE)-grown P4 cultures. While such metabolic flexibility could impart physiological advantage in sustaining P-starvation stress, it manifests as unique coexistence of P-solubilizing and biocontrol abilities.