Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato)

Abstract

BackgroundResearch to understand and control microbiological risks associated with the consumption of fresh fruits and vegetables has examined many environments in the farm to fork continuum. An important data gap however, that remains poorly studied is the baseline description of microflora that may be associated with plant anatomy either endemically or in response to environmental pressures. Specific anatomical niches of plants may contribute to persistence of human pathogens in agricultural environments in ways we have yet to describe. Tomatoes have been implicated in outbreaks of Salmonella at least 17 times during the years spanning 1990 to 2010. Our research seeks to provide a baseline description of the tomato microbiome and possibly identify whether or not there is something distinctive about tomatoes or their growing ecology that contributes to persistence of Salmonella in this important food crop.ResultsDNA was recovered from washes of epiphytic surfaces of tomato anatomical organs; leaves, stems, roots, flowers and fruits of Solanum lycopersicum (BHN602), grown at a site in close proximity to commercial farms previously implicated in tomato-Salmonella outbreaks. DNA was amplified for targeted 16S and 18S rRNA genes and sheared for shotgun metagenomic sequencing. Amplicons and metagenomes were used to describe “native” bacterial microflora for diverse anatomical parts of Virginia-grown tomatoes.ConclusionsDistinct groupings of microbial communities were associated with different tomato plant organs and a gradient of compositional similarity could be correlated to the distance of a given plant part from the soil. Unique bacterial phylotypes (at 95% identity) were associated with fruits and flowers of tomato plants. These include Microvirga, Pseudomonas, Sphingomonas, Brachybacterium, Rhizobiales, Paracocccus, Chryseomonas and Microbacterium. The most frequently observed bacterial taxa across aerial plant regions were Pseudomonas and Xanthomonas. Dominant fungal taxa that could be identified to genus with 18S amplicons included Hypocrea, Aureobasidium and Cryptococcus. No definitive presence of Salmonella could be confirmed in any of the plant samples, although 16S sequences suggested that closely related genera were present on leaves, fruits and roots.

Environmental Metabolomics of the Tomato Plant Surface Provides Insights on Salmonella enterica Colonization

“…tomato (22). Overall, evidence points to a heterogeneous phyllosphere (23) supporting a complex microbiome (20) with significant plantdriven regulation, partly mediated by plant metabolites and exudates. Specifically for S. enterica, population sizes on lettuce leaf surfaces have been correlated with the availability of nitrogen in leaf exudates (24), and S. enterica movement toward sugar compounds in lettuce root exudates is driven by chemotaxis (25).…”

“…Exudation via roots alters the chemical and physical properties of soil in their immediate vicinity to form the rhizosphere, influencing microbial recruitment (16)(17)(18). Plant-driven bacterial selection has also been noted in the tomato phyllosphere (19), and plant organspecific microbiomes have been described (20), although they have not yet been linked to plant surface compounds. Soluble carbohydrates and phenolics from homogenized leaf material of a variety of lettuce accessions have been associated with shifts in lettuce phyllosphere bacterial community fingerprints (21), and metabolic pathways are turned on to enable utilization of tomato apoplastic nutrients in Pseudomonas syringae pv.…”

Xanthomonas perforans Colonization Influences Salmonella enterica in the Tomato Phyllosphere

“…Nontyphoid salmonellosis outbreaks have occurred annually over the last decade due to the contamination of a variety of edible plants by various serovars of S. enterica. Outbreaks associated with S. enterica contamination of tomato consistently occur in agricultural areas where the pathogen is now considered endemic (2). S. enterica appears to establish reservoirs on plants and to use them as vectors to animals, a preferred host (3).…”

Genomics of Specificity in the Symbiotic Interaction between Rhizobium leguminosarum and Legumes

“…We further argue that any rhizobial Lundberg et al, 2012, Chaparro et al, 2013, Ottesen et al, 2013, Schlaeppi et al, 2013, Tkacz et al, 2015, Yeoh et al, 2015.…”

“…Furthermore, characterizing soil rhizobia independently of their plant symbiotic phenotypes allowed us to uncover a large and diverse population of nonsymbiotic rhizobia whose existence had been known, but whose size and variability had not been studied. This "invisible" rhizobial population is, nonetheless, important for two reasons: a) they can be donors or recipients of genetic material to or from symbiotic rhizobia in horizontal gene transfer events, thus acting as an important pangenomic reservoir; and b) they can influence plant nutrition, growth and development not only of compatible legumes, but also of many other plants, in what is being uncovered as a major new role of non-symbiotic rhizobia as widespread constituents of plant microbiomes (Lundberg et al, 2012, Chaparro et al, 2013, Ottesen et al, 2013, Schlaeppi et al, 2013, Tkacz et al, 2015, Yeoh et al, 2015.…”