Xanthomonas perforans Colonization Influences Salmonella enterica in the Tomato Phyllosphere

Salmonella enterica is a member of the plant microbiome. Growth of S. enterica in sprouting-seed exudates is rapid; however, the active metabolic networks essential in this environment are unknown. To examine the metabolic requirements of S. enterica during growth in sprouting-seed exudates, we inoculated alfalfa seeds and identified 305 S. enterica proteins extracted 24 h postinoculation from planktonic cells. Over half the proteins had known metabolic functions, and they are involved in over onequarter of the known metabolic reactions. Ion and metabolite transport accounted for the majority of detected reactions. Proteins involved in amino acid transport and metabolism were highly represented, suggesting that amino acid metabolic networks may be important for S. enterica growth in association with roots. Amino acid auxotroph growth phenotypes agreed with the proteomic data; auxotrophs in amino acid-biosynthetic pathways that were detected in our screen developed growth defects by 48 h. When the perceived sufficiency of each amino acid was expressed as a ratio of the calculated biomass requirement to the available concentration and compared to growth of each amino acid auxotroph, a correlation between nutrient availability and bacterial growth was found. Furthermore, glutamate transport acted as a fitness factor during S. enterica growth in association with roots. Collectively, these data suggest that S. enterica metabolism is robust in the germinating-alfalfa environment; that single-amino-acid metabolic pathways are important but not essential; and that targeting central metabolic networks, rather than dedicated pathways, may be necessary to achieve dramatic impacts on bacterial growth. P lants can influence both the number and species of bacteria that colonize their surfaces. The availability and types of nutrients, secretion of chemoattractants or repellents, and production of antimicrobial compounds all impact the composition of the plant-associated bacterial community. In particular, germinating seeds and roots release exudates containing complex mixtures of amino acids, sugars, organic acids, and other plant metabolites that support the growth of microbial colonists in the spermosphere and rhizosphere (1-5). Successful colonization of and persistence in these plant niches requires that bacteria acquire and metabolize these plant-derived nutrients and biosynthesize any required metabolites not sufficiently available from the plant.The compositions of seed and root exudates are dynamic and vary based on seed and plant age, soil type, temperature, nutritional status, and crop (6, 7). The identity and quantity of nutrients in plant exudates have a profound impact on bacterial growth and metabolic activity (8). Seeds that released larger quantities of carbohydrates and amino acids supported higher Enterobacter cloacae populations, rates of bacterial growth, and metabolic activity (3,4,8). Nutrient identity (e.g., alanine, arginine, and aspartate), not just type (e.g., amino acids, sugars, and lipids), influen...

mentioning

confidence: 81%

De Novo Amino Acid Biosynthesis Contributes to Salmonella enterica Growth in Alfalfa Seedling Exudates

Kwan

Pisithkul

Amador‐Noguez

et al. 2015

“…The bacterium, when either applied to the surface of the fruit or inoculated into the stem scar or the pulp itself, can survive and proliferate (11)(12)(13)(14)(15). It can also survive on leaves in the absence of desiccation (16) and proliferates significantly better when coinoculated with a bacterial plant pathogen (14,(17)(18)(19). Also important to our work is the finding that Salmonella enterica serovar Montevideo, which has been the cause of human outbreaks and is used in our studies, survives well in ripe tomatoes (12,13,16).…”

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confidence: 99%

Acquisition of Iron Is Required for Growth of Salmonella spp. in Tomato Fruit

Nugent

Meng

Martin

et al. 2015

c Salmonella remains a leading cause of bacterial food-borne disease, sickening millions each year. Although outbreaks of salmonellosis have traditionally been associated with contaminated meat products, recent years have seen numerous disease cases caused by the consumption of produce. Tomatoes have been specifically implicated, due to the ability of Salmonella spp. to enter the tomato fruit and proliferate within, making the decontamination of the raw product impossible. To investigate the genetic means by which Salmonella is able to survive and proliferate within tomatoes, we conducted a screen for bacterial genes of Salmonella enterica serovar Montevideo specifically induced after inoculation into ripe tomato fruit. Among these genes, we found 17 members of the previously described anaerobic Fur (ferric uptake regulator) regulon. Fur is a transcriptional and posttranscriptional regulator known to sense iron, suggesting the importance of this mineral to Salmonella within tomatoes. To test whether iron acquisition is essential for Salmonella growth in tomatoes, we tested a ⌬fepDGC mutant, which lacks the ability to import iron-associated siderophores. This mutant grew significantly more poorly within tomatoes than did the wild type, but the growth defect of the mutant was fully reversed by the addition of exogenous iron, demonstrating the need for bacterial iron scavenging. Further, dependence upon iron was not apparent for Salmonella growing in filtered tomato juice, implicating the cellular fraction of the fruit as an important mediator of iron acquisition by the bacteria.

“…Plant pathogens carry a set of virulence factors that inhibit the plant innate immune responses so that bacteria can grow on and colonize the phyllosphere. Recently, we discovered that Xanthomonas perforans influences S. enterica survival in the tomato phyllosphere (7). Via the type 3 secretion system, virulent X. perforans modifies the phyllosphere, resulting in susceptibility, which in turn increases the persistence of S. enterica on infected leaves.…”

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confidence: 99%

“…During initial immigration events, pathogens and other phyllosphere colonizers that land at protected sites, such as veins, trichomes, and stomata, manage to avoid some stresses. S. enterica has been shown to preferentially colonize trichomes (6) and has been found near stomata (7), which might offer them sites for protection against stresses as well as make resources available.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Plant Pathogen-Induced Water-Soaking Promotes Salmonella enterica Growth on Tomato Leaves

Potnis

Colee

Jones

et al. 2015

Self Cite

c Plant pathogen infection is a critical factor for the persistence of Salmonella enterica on plants. We investigated the mechanisms responsible for the persistence of S. enterica on diseased tomato plants by using four diverse bacterial spot Xanthomonas species that differ in disease severities. Xanthomonas euvesicatoria and X. gardneri infection fostered S. enterica growth, while X. perforans infection did not induce growth but supported the persistence of S. enterica. X. vesicatoria-infected leaves harbored S. enterica populations similar to those on healthy leaves. Growth of S. enterica was associated with extensive water-soaking and necrosis in X. euvesicatoria-and X. gardneri-infected plants. The contribution of water-soaking to the growth of S. enterica was corroborated by an increased growth of populations on water-saturated leaves in the absence of a plant pathogen. S. enterica aggregates were observed with bacterial spot lesions caused by either X. euvesicatoria or X. vesicatoria; however, more S. enterica aggregates formed on X. euvesicatoria-infected leaves as a result of larger lesion sizes per leaf area and extensive watersoaking. Sparsely distributed lesions caused by X. vesicatoria infection do not support the overall growth of S. enterica or aggregates in areas without lesions or water-soaking; S. enterica was observed as single cells and not aggregates. Thus, pathogeninduced water-soaking and necrosis allow S. enterica to replicate and proliferate on tomato leaves. The finding that the pathogen-induced virulence phenotype affects the fate of S. enterica populations in diseased plants suggests that targeting of plant pathogen disease is important in controlling S. enterica populations on plants.