The soilborne pathogen Ralstonia solanacearum causes a lethal bacterial wilt disease of tomato and many other crops by infecting host roots, then colonizing the water-transporting xylem vessels. Tomato xylem sap is nutritionally limiting but it does contain some carbon sources, including sucrose, trehalose, and myo-inositol. Transcriptomic analyses revealed that R. solanacearum expresses distinct 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 in planta fitness of bacterial mutants lacking specific carbon catabolic pathways expressed at either LCD or HCD. We hypothesized that early in disease, during root infection, the bacterium depends on carbon sources catabolized at LCD, while HCD carbon sources are only required later in disease during stem colonization. A R. solanacearum ΔiolG mutant unable to use the LCD-catabolized nutrient myo-inositol was defective in tomato root colonization, but after it reached the stem this strain colonized and caused symptoms as well as wild type. In contrast, R. solanacearum mutants unable to use the HCD-catabolized nutrients sucrose (ΔscrA), trehalose (ΔtreA), or both (ΔscrA/treA), infected roots as well as wild-type R. solanacearum but were defective in colonization and competitive fitness in midstems and had reduced virulence. Further, xylem sap from tomato plants colonized by ΔscrA, ΔtreA, or ΔscrA/treA R. solanacearum mutants contained twice as much sucrose as sap from plants colonized by wild-type R. solanacearum. Together, these findings suggest that quorum sensing specifically adapts R. solanacearum metabolism for success in the different nutritional environments of plant roots and xylem sap.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

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