Ralstonia solanacearum depends on catabolism of myo-inositol, sucrose, and trehalose for virulence in an infection stage-dependent manner

Abstract

The soilborne pathogen Ralstonia solanacearum (Rs) causes lethal bacterial wilt disease of tomato and many other crops by infecting host roots and then colonizing the xylem vessels. Tomato xylem sap is nutritionally limiting but it does contain sucrose and trehalose. Transcriptomic analyses revealed that Rs expresses distinct sets of catabolic pathways at low cell density (LCD) and high cell density (HCD). To investigate the links between bacterial catabolism, infection stage, and virulence, we measured the in planta fitness of bacterial mutants lacking carbon catabolic pathways expressed at either LCD or HCD. We hypothesized that the bacterium needs LCD carbon sources early in disease (root infection) while HCD carbon sources are required during late disease (stem colonization). An Rs ΔiolG mutant unable to use the LCD nutrient myo-inositol was defective in root colonization but once it reached the stem, this strain colonized and caused symptoms as well as wild type. In contrast, Rs mutants unable to use sucrose (ΔscrA), trehalose (ΔtreA), or both (ΔscrA/treA), infected roots as well as wild type but were defective in colonization and competitive fitness in tomato mid-stems and were reduced in bacterial wilt virulence. Additionally, xylem sap from tomato plants colonized by ΔscrA, ΔtreA, or ΔscrA/treA contained more sucrose than sap from plants colonized by wild-type Rs. Together, these findings suggest Rs metabolism is specifically adapted for success in the different nutritional environments of plant roots and xylem sap.