SALMONELLA ENTERICA INTERACTIONS WITH TOMATO: PLANT GENOTYPE EFFECTS AND SALMONELLA GENETIC RESPONSES

Abstract

Several outbreaks of Salmonella enterica infections have been linked to tomatoes. One cost-effective way to complement on-farm preventive Good Agricultural Practices would be to identify cultivars with inherent decreased susceptibility to Salmonella colonization. Various tomato cultivars with distinct phenotypes were screened to evaluate their susceptibility to Salmonella epiphytic colonization. The potential role of plant exudates, collected from the same cultivars, on the growth kinetics of Salmonella was examined. These investigations were supplemented with Salmonella genome-wide transcriptomics that showed bacterial responses to colonization of tomato shoots and roots. Epiphytic colonization of fruit by S. enterica was cultivar-dependent and serotype-specific, but did not correlate with leaf colonization. Fruit and leaves of the same cultivar differed in their ability to support Salmonella growth. Quantitative and qualitative analysis of tomato exudates provided a possible explanation for the differential susceptibility to bacterial colonization among tomato cultivars. Tomato exudates alone were capable of supporting Salmonella growth, and the growth kinetics of Salmonella in tomato exudates differed by cultivar. Characterization of the chemical composition of primary and secondary metabolites in tomato exudates pointed to potential causes for the differential growth of Salmonella observed in the exudates of various tomato cultivars. Key transcriptomic signals that were down- and up-regulated in Salmonella upon interacting with tomato were identified, enabling us to elucidate the molecular mechanisms underlying this enteric pathogen-plant interaction. Overall, the identified signals lead to a proposed model that depicts the cellular processes needed to preserve cell viability when multiple abiotic stresses in conjunction with low nutrient availability are encountered, while simultaneously repressing unnecessary energy demands or maintaining them at a level equivalent to growth in a nutritious medium. These findings strongly support the hypothesis that plant-regulated mechanisms influence enteric pathogen colonization. It is clear that Salmonella can sense subtle environmental cues brought about by the genotype or physiological state of plants and can respond with distinct patterns of gene expression. Future work should focus on whether this bacterial behavior on plants results from an evolutionary adaptation to use plants as a vector to re-enter animal hosts.