Ralstonia solanacearumdepends 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 (∆scrA/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.

Trehalose Synthesis Contributes to Osmotic Stress Tolerance and Virulence of the Bacterial Wilt PathogenRalstonia solanacearum

“…The existence of the type III-secreted effector TPS (RipTPS) also hints at an active pathogen role in manipulating plant trehalose metabolism (Poueymiro et al 2014). However, although strain GMI1000 can grow on trehalose as a sole carbon source, this sugar is not a significant carbon source for R. solanacearum during tomato colonization and pathogenesis, and trehalose is present in xylem sap at much lower concentrations than the more palatable sucrose (Hamilton et al 2019).…”

“…Quantitative PCR measurement of treY, treS, and otsA expression in a treA mutant background showed that mutating trehalase did not affect expression of any of the trehalose biosynthetic pathways, suggesting trehalose synthesis is regulated independently from its degradation (data not shown). Further characterization of the DtreA mutant is reported elsewhere (Hamilton et al 2019). The DotsA and DtreY/treS/otsA strains grew as well as wild type in minimal media plus glucose at the R. solanacearum optimal growth temperature of 28°C ( Fig.…”

Nitric Oxide Regulates theRalstonia solanacearumType 3 Secretion System

“…Mutating any of these genes leads to a loss of T3SS gene expression, yet all three were highly downregulated in planta compared to either CPG or VDM ( Supplementary Table 4) (Zhang et al 2011;Jacobs et al 2012). Several other genes that were highly upregulated in planta in both experiments encode metabolism of sucrose or myo-inositol, two carbon sources important for R. solanacearum during infection (Lowe-Power et al 2018b;Hamilton et al 2020;Xian et al 2020). Additionally, genes involved in flagellar motility were upregulated in both experiments.…”

“…solanacearum during infection (Hamilton et al, 2020;Lowe-Power, Khokhani, et al, 2018;Xian et al, 2020). Additionally, genes involved in flagellar motility were upregulated in both experiments.…”

Trehalose increases tomato drought tolerance, induces defenses, and increases resistance to bacterial wilt disease

“…No reuse allowed without permission. R. solanacearum GMI1000 produces and secretes abundant amounts of the TreA trehalase during tomato infection, and ability to degrade trehalose contributes to bacterial fitness and virulence even though trehalose is not an important nutritional source for the pathogen (Jacobs, Babujee et al 2012, Hamilton, Steidl et al 2021. Interestingly, treating plants with the trehalase inhibitor Validamycin A increased BW resistance (Ishikawa, Fujimori et al 1996).…”