Interaction between Salmonella and Plants: Potential Hosts and Vectors for Human Infection

Fruits and vegetables are important for a healthy diet. However, when eaten raw and contaminated with human pathogens (HPs) they may cause a disease outbreak. Contamination with HPs can occur along the entire farm-to-fork production chain and Salmonella enterica is one of the most common foodborne pathogens. A range of biotic and abiotic environmental factors can influence the complex interactions between Salmonella and plants. Moreover, the outcome of experiments largely depends on the experimental design and parameters or methods employed, and on top, on the accompanying plant microbiome and the genetic equipment of the plant and the Salmonella strain. Particularly mobile genetic elements contribute to the diversification and adaptation of Salmonella to the plant environment. So far, little is known about the key processes and factors influencing the attachment and potential internalization of Salmonella in plants and the plant specific responses. It is therefore important to better understand the ecology of Salmonella in the soil and plant environment, in order to propose practicable recommendations for prevention of foodborne diseases. This also requires improved sensitivity and specificity of detection methods. In this chapter, we present the current knowledge, research needs, and methodology regarding the complex interactions between Salmonella and plants

Salmonella enterica relies on carbon metabolism to adapt to agricultural environments

Salmonella enterica, a foodborne and human pathogen, is a constant threat to human health. Agricultural environments, for example, soil and plants, can be ecological niches and vectors for Salmonella transmission. Salmonella persistence in such environments increases the risk for consumers. Therefore, it is necessary to investigate the mechanisms used by Salmonella to adapt to agricultural environments. We assessed the adaptation strategy of S. enterica serovar Typhimurium strain 14028s to agricultural-relevant situations by analyzing the abundance of intermediates in glycolysis and the tricarboxylic acid pathway in tested environments (diluvial sand soil suspension and leaf-based media from tomato and lettuce), as well as in bacterial cells grown in such conditions. By reanalyzing the transcriptome data of Salmonella grown in those environments and using an independent RT-qPCR approach for verification, several genes were identified as important for persistence in root or leaf tissues, including the pyruvate dehydrogenase subunit E1 encoding gene aceE. In vivo persistence assay in tomato leaves confirmed the crucial role of aceE. A mutant in another tomato leaf persistence-related gene, aceB, encoding malate synthase A, displayed opposite persistence features. By comparing the metabolites and gene expression of the wild-type strain and its aceB mutant, fumarate accumulation was discovered as a potential way to replenish the effects of the aceB mutation. Our research interprets the mechanism of S. enterica adaptation to agriculture by adapting its carbon metabolism to the carbon sources available in the environment. These insights may assist in the development of strategies aimed at diminishing Salmonella persistence in food production systems

Composted sewage sludge influences the microbiome and persistence of human pathogens in soil

Composted sewage sludge (CSS) gained attention as a potential fertilizer in agriculture. Application of CSS increases soil microbial activity and microbial biomass, however, it can also lead to increased chemical and microbiological risks. In this study, we performed microcosm experiments to assess how CSS reshapes the microbial community of diluvial sand (DS) soil. Further, we assessed the potential of CSS to increase the persistence of human pathogens in DS soil and the colonization of Chinese cabbage (Brassica rapa L. subsp. pekinensis (Lour.) Hanelt). The results revealed that CSS substantially altered the prokaryotic community composition. Moreover, addition of CSS increased the persistence of Salmonella enterica serovar Typhimurium strain 14028s and S. enterica serovar Senftenberg in DS soil. However, the enhanced persistence in soil had no impact on the colonization rate of B. rapa grown on soil inoculated with Salmonella. We detected Salmonella in leaves of 1.9% to 3.6% of plants. Addition of CSS had no impact on the plant colonization rate. The use of sewage sludge composts is an interesting option. However, safety measures should be applied in order to avoid contamination of crop plants by human pathogens

Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species

Human pathogenic bacteria, such as Salmonella enterica, are able to colonize crop plants. So far, not much is known about biotic and abiotic factors influencing this colonization in field soil. This understanding, however, is imperative for the provision of safe fresh produce to the consumer. In this study, we investigated the effects of soil type, organic fertilization, plant species and the way of Salmonella entry into the plant production system, on the survival of S. enterica in soil as well as the colonization of plants. The selected S. enterica serovar Typhimurium strain 14028s, S. Typhimurium strain LT2 and S. Senftenberg were able to persist in soil for several weeks. Salmonella’s persistence in soil was prolonged in loamy, if compared to sandy soil, and when applied together with organic fertilizer. The leaves of lettuce and corn salad were colonized by S. enterica providing evidence for internalization from the soil via the root. Colonization rates were affected by soil type, plant species and S. enterica strain. Overall, S. enterica was detected in leaves of 0.5–0.9% of the plants, while lettuce was more frequently colonized than corn salad. Plants grown in sandy soil were more often colonized than plants grown in loamy soil. After spray inoculation, S. enterica could be detected on and in leaves for several weeks by cultivation-depending methods, confirmed by confocal microscopy using GFP-labeled S. Typhimurium 14028s. On the one hand, transcriptome data from S. Typhimurium 14028s assessed in response to lettuce medium or lettuce root exudates showed an upregulation of genes associated with biofilm formation and virulence. On the other hand, lettuce inoculated with S. Typhimurium 14028s showed a strong upregulation of genes associated with plant immune response and genes related to stress response. In summary, these results showed that organic fertilizers can increase the persistence of Salmonella in soil and that soil type and plant species play a crucial role in the interactions between human pathogens and crop plants. This understanding is therefore a starting point for new strategies to provide safe food for the consumer

Hordeum vulgare differentiates its response to beneficial bacteria

Background In nature, beneficial bacteria triggering induced systemic resistance (ISR) may protect plants from potential diseases, reducing yield losses caused by diverse pathogens. However, little is known about how the host plant initially responds to different beneficial bacteria. To reveal the impact of different bacteria on barley (Hordeum vulgare), bacterial colonization patterns, gene expression, and composition of seed endophytes were explored. Results This study used the soil-borne Ensifer meliloti, as well as Pantoea sp. and Pseudomonas sp. isolated from barley seeds, individually. The results demonstrated that those bacteria persisted in the rhizosphere but with different colonization patterns. Although root-leaf translocation was not observed, all three bacteria induced systemic resistance (ISR) against foliar fungal pathogens. Transcriptome analysis revealed that ion- and stress-related genes were regulated in plants that first encountered bacteria. Iron homeostasis and heat stress responses were involved in the response to E. meliloti and Pantoea sp., even if the iron content was not altered. Heat shock protein-encoding genes responded to inoculation with Pantoea sp. and Pseudomonas sp. Furthermore, bacterial inoculation affected the composition of seed endophytes. Investigation of the following generation indicated that the enhanced resistance was not heritable. Conclusions Here, using barley as a model, we highlighted different responses to three different beneficial bacteria as well as the influence of soil-borne Ensifer meliloti on the seed microbiome. In total, these results can help to understand the interaction between ISR-triggering bacteria and a crop plant, which is essential for the application of biological agents in sustainable agriculture