Trophic preferences of the pathogen Ralstonia solanacearum and consequences on its growth in xylem sap

Abstract

Ralstonia solanacearum is one of the most destructive pathogens worldwide. In the last 30 years, the molecular mechanisms at the origin of R. solanacearum pathogenicity have been studied in depth. However, the nutrition status of the pathogen once inside the plant has been poorly investigated. Yet, the pathogen needs substrates to sustain a fast‐enough growth, maintain its virulence and subvert the host immunity. This study aimed to explore in‐depth the xylem environment where the pathogen is abundant, and its trophic preferences. First, we determined the composition of tomato xylem sap, where fast multiplication of the pathogen occurs. Then, kinetic growth on single and mixtures of carbon sources in relation to this environment was performed to fully quantify growth. Finally, we calculated the concentration of available metabolites in the xylem sap flux to assess how much it can support bacterial growth in planta . Overall, the study underlines the adaptation of R. solanacearum to the xylem environment and the fact that the pathogen assimilates several substrates at the same time in media composed of several carbon sources. It also provides metrics on key physiological parameters governing the growth of this major pathogen, which will be instrumental in the future to better understand its metabolic behavior during infection.

Plant pathogenicRalstoniaphylotypes evolved divergent respiratory strategies and behaviors to thrive in xylem

“…Plant xylem has often been described as a nutrient-poor environment (9). However, recent quantitative metabolomics and physiological modeling shows that healthy tomato xylem sap contains enough organic carbon and nitrogen to sustain Ralstonia’ s rapid growth, including mM levels of amino acids and 0.1 mM levels of glucose and sucrose (12, 13). Xylem sap should thus be considered a rich, but incomplete, medium (37).…”

“…In vitro experiments indicate that phyl. I strain GMI1000 relies primarily on the glutamate, asparagine, aspartate, and glucose in xylem (12, 13). Catabolism of other sugars contribute slightly to success in xylem (11).…”

“…The physiology of the model phyl. I strain GMI1000 has been extensively studied (3,(8)(9)(10)(11)(12)(13)(14), but little is known about core metabolism in other plant pathogenic Ralstonia. Using a genetically diverse panel of RSSC strains, we showed that phylotypes I and III (hereafter phyl.…”

Insights into the metabolic specificities of pathogenic strains from theRalstonia solanacearum species complex

“…To date, the metabolism and trophic preferences (i.e. the identification of the metabolic substrates preferentially metabolized by a strain) were studied only in GMI1000 strain (16, 17). The metabolic network of R. pseudosolanacearum strain GMI1000 was reconstructed (16), which first provided a global view of the strains’ metabolism and catabolic capacities.…”

“…PhcA thus appears as a major regulator of both virulence and metabolism. Finally, the mapping of the substrates preferentially metabolized by the GMI1000 strain was carried out, thus allowing the identification of the compounds that sustain fast bacterial growth and were likely to be assimilated in tomato xylem sap (17).…”