Salmonella adapts to plants and their environment during colonization of tomatoes

Abstract

Humans and animals are considered typical hosts for Salmonella, however, also plants can be colonized. Tomatoes were linked to salmonellosis outbreaks already on several occasions. The aim of this study was, therefore, to establish a comprehensive view on the interaction between Salmonella enterica and tomatoes, and to test the hypothesis that colonization of plants is an interactive process. We assessed the persistence of Salmonella in agricultural soil, the colonization pattern in and on tomatoes, as well as the reciprocal responses of tomatoes to different Salmonella strains and Salmonella to root exudates and tomato-related media. This study revealed that Salmonella can persist in the soil and inside the tomato plant. Additionally, we show that Salmonella strains have particular colonization pattern, although the persistence inside the plant differs between the tested strains. Furthermore, the transcriptome response of tomato showed an up-regulation of several defense-related genes. Salmonella transcriptome analysis in response to the plant-based media showed differentially regulated genes related to amino acid and fatty acid synthesis and stress response, while the response to root exudates revealed regulation of the glyoxylate cycle. Our results indicate that both organisms actively engage in the interaction and that Salmonella adapts to the plant environment.

Salmonella Heterogeneously Expresses Flagellin during Colonization of Plants

“…We observed no differences in the number of CFU recovered from leaves inoculated with the S. Typhimurium ∆fljB∆fliC mutant strain versus those from leaves inoculated with the wild type S. Typhimurium 14028s (Figure 1a). These results are in line with our previous reports of Salmonella persistence in tomato plants [27], and indicate that the presence of functional flagella is not required for persistence of Salmonella in plants. Growth of both strains was also very similar in tomato-based medium (TM) ( Figure 1b) [27].…”

“…Bacteria were grown in Luria-Bertani (LB) broth (Carl Roth GmbH & Co., KG, Karlsruhe, Germany) or on LB agar plates. Plant-based media, namely lettuce medium (LM) and tomato medium (TM), were prepared as described previously by [26,27], respectively. Minimal medium (MM) was used as a control medium and was prepared as described by [27].…”

“…Plant-based media, namely lettuce medium (LM) and tomato medium (TM), were prepared as described previously by [26,27], respectively. Minimal medium (MM) was used as a control medium and was prepared as described by [27]. Xylose-lysine-desoxycholate (XLD) agar (Carl Roth GmbH & Co., KG) was used as a selective medium for Salmonella.…”

“…To evaluate this possibility, expression of flagellin-coding fljB and fliC genes was determined first in media supplemented with plant extracts. Expression levels for these two genes were assessed at three different time points during bacterial replication in tomato-based medium (TM) [27] and, to evaluate a potential influence of diverse plant environments, expression was also assessed in lettuce-originated medium (LM) [29], as well as in a minimal medium (MM) with similar composition to TM and LM media but without added plant extracts. LB medium was used as a reference.…”

“…To get further data on this issue, we monitored the response of tomato plants to spray-inoculation with wild type S. Typhimurium 14028s and the S. Typhimurium ∆fljB∆fliC double mutant. Expression of five defense-associated marker genes, CHI3, CHI9, GlucA, GlucB [27] and FRK1.1 was analyzed. Expression of all genes (except for FRK1.1) was induced 6 h post inoculation, but no significant differences in the plant response were detected after inoculation with either strain (Figure 7).…”