Unique Metabolic Reprogramming in Pseudomonas Aeruginosa P4 Facilitates the Unusual Concurrence of P-solubilizing and Biocontrol Traits Under P-limitation

Abstract

Plant-beneficial fluorescent Pseudomonas species with concurrent P–solubilizing and biocontrol traits could have improved rhizospheric survival and efficacy; although this rare ability is subject to diverse environmental and endogenous regulations. This study investigates the P-limitation-induced regulations enabling co-production of metabolites implied in P-solubilization and biocontrol by P. aeruginosa P4 (P4). P-limitation reduced the growth rate of P4 while metabolic distribution of total glucose depleted shifted to increased periplasmic gluconic acid production. Remarkably, despite a parallel reduction in glucose consumption, the production of biocontrol metabolites like pyocyanin, total siderophores and IAA enhanced under P-solubilizing conditions. The study indicates a metabolic rearrangement in P4 under P-limitation such that biomass yield is maintained while adjusting the chorismate-mediated secondary metabolism. A time course analysis on glucose and artificial root exudates, unusually reduced aroC expression (encoding the rate-limiting enzyme chorismate synthase) and growth phase-dependent changes in the expression of key biosynthetic genes pchA, pchE, pchG, pvdQ and phzM suggested that although the enhanced production of chorismate-derived secondary metabolites could be attributed to P-limitation, the underlying gene expression could be governed by multiple factors. While such metabolic flexibility could impart physiological advantage in sustaining P-starvation stress, it manifests as unique coexistence of P-solubilizing and biocontrol abilities.