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Food Microbiology | Spotlight

Salad Leaf Juices Enhance Salmonella Growth, Colonization of Fresh Produce, and Virulence

Giannis Koukkidis, Richard Haigh, Natalie Allcock, Suzanne Jordan, Primrose Freestone
Johanna Björkroth, Editor
Giannis Koukkidis
aDepartment of Infection, Immunity and Inflammation, University of Leicester, Leicester, United Kingdom
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Richard Haigh
bDepartment of Genetics, University of Leicester, Leicester, United Kingdom
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Natalie Allcock
cCore Biotechnology Services, University of Leicester, Leicester, United Kingdom
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Suzanne Jordan
dCampden BRI, Chipping Campden, Gloucestershire, United Kingdom
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Primrose Freestone
aDepartment of Infection, Immunity and Inflammation, University of Leicester, Leicester, United Kingdom
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Johanna Björkroth
University of Helsinki
Roles: Editor
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DOI: 10.1128/AEM.02416-16
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    FIG 1

    Salad extracts induce Salmonella growth in water. (A) In vitro time course of growth at 37°C of Salmonella in water with increasing levels of spinach juice; values shown are means from triplicate time points; n = 3. (B) Images showing the fluid that accumulates in bagged salads, spinach, and mixed-leaf varieties. (C) Histograms showing the in vitro growth at 4°C of 101 CFU/ml Salmonella inoculated into sterile water supplemented with 5% to 20% (vol/vol) doses of fluids from a spinach and mixed-leaf salad bag; values shown are means from triplicate time points; n = 3. *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

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    FIG 2

    Salad extracts increase Salmonella motility and biofilm formation. (A) Salmonella motility at room temperature in 2% (vol/vol) salad leaf juice-supplemented DMEM relative to unsupplemented controls (P ≤ 0.01). Key: C, control (no additions); Cl, cos lettuce; Bo, baby green oak lettuce; Rr, red romaine lettuce; S, spinach; Rc, red chard; n = 5. (B) Initial in vitro attachment of Salmonella in water in the presence of salad juice relative to unsupplemented controls (P ≤ 0.001). Initial inocula were 106 CFU/ml; values shown are means of 4 data points; n = 3. Key: C, control (no additions); Cl, cos lettuce; Bo, baby green oak lettuce; Rr, red romaine lettuce; S, spinach; Rc, red chard. The various leaf juices were supplemented as 2% (vol/vol) additions; n = 3. (C) Light microscopy image showing biofilm formation of Salmonella treated for 4 and 18 h with incubation at room temperature with 2% spinach juice–DMEM; n = 6. (D) Histogram showing that 2% spinach extract in water enhances Salmonella attachment to spinach leaves after a 30-min incubation at room temperature; values shown are means of 6 data points; n = 3. **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

  • FIG 3
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    FIG 3

    Spinach juice increases Salmonella colonization of salad leaves. (A) Representative scanning electron micrographs of untreated (−) and 2% (vol/vol) spinach juice-exposed (+) Salmonella seeded at 105 CFU/ml onto 5-by-5-mm sections of spinach leaves as described in Materials and Methods. (B) Attachment profiles of the leaf microbiota in the absence (−) and presence (+) of 2% (vol/vol) spinach juice; n = 3. Scale bars are shown in white at the bottom of each set of images. (C) In vitro growth responses of the salad leaf microbiota (inoculated at 102 CFU/ml) to spinach juice (2%) and spinach bag fluid (20%); P > 0.05; n = 8.

  • FIG 4
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    FIG 4

    Salad juice increases colonization of salad bags by Salmonella. (A and B) Typical pictures of a salad bag microbiota. Panel A shows microbes growing from the salad bag and panel B the diversity of microbes transferred from a bag imprint onto Luria agar. (C) Light microscopy images of Salmonella (seeded at 105 CFU/ml) and endogenous microbiota colonization of salad bag plastic in water in the absence (−) and presence (+) of 2% spinach juice; images were captured using a light microscope (bright field) set at ×60 magnification; n = 8. (D) Blue light microscopy images (×60 magnification) of 105 CFU/ml GFP-Salmonella incubated in water in the absence (Control) and presence of 2% spinach juice or 20% spinach bag fluid; n = 3.

  • FIG 5
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    FIG 5

    Salad bag fluids enhance Salmonella growth in host-like media. (A) Histograms showing the salad juice response growth responses of Salmonella in serum-SAPI medium. Bacteria were inoculated at 102 CFU/ml and incubated for 18 h at 37°C. Values shown are means of 6 data points; relative to controls, all data values have a P value of ≤0.001; n = 3. Key: C, control (no additions); Cl, cos lettuce; Bo, baby green oak lettuce; Rr, red romaine lettuce; S, spinach; Rc, red chard. (B) Urea gel showing that salad extracts (2% vol/vol) can remove iron from holo-transferrin (Holo); n = 5. Key: C, control (no additions); Cl, cos lettuce; Bo, baby green oak lettuce; Rr, red romaine lettuce; S, spinach; Rc, red chard. (C) Histograms showing the uptake of transferrin-complexed 55Fe by Salmonella in the absence and presence of 2% spinach juice (Juice) (P ≤ 0.0001) and 20% spinach bag fluid (Bag fluid) (P ≤ 0.001; n = 3). (D) Histograms comparing the serum-SAPI growth response profile at 37°C of a Salmonella enterobactin mutant with that of the wild type in the presence of salad juice and salad leaf dietary catechols. Values shown are means from 3 data points; n = 3. Key: C, control (no additions); S, 2% (vol/vol) spinach juice; Fe, 100 μM ferric nitrate; Ta, 100 μM tannic acid; Ca, 100 μM chlorogenic acid. **, P ≤ 0.01; ****, P ≤ 0.0001.

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Salad Leaf Juices Enhance Salmonella Growth, Colonization of Fresh Produce, and Virulence
Giannis Koukkidis, Richard Haigh, Natalie Allcock, Suzanne Jordan, Primrose Freestone
Applied and Environmental Microbiology Dec 2016, 83 (1) e02416-16; DOI: 10.1128/AEM.02416-16

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Salad Leaf Juices Enhance Salmonella Growth, Colonization of Fresh Produce, and Virulence
Giannis Koukkidis, Richard Haigh, Natalie Allcock, Suzanne Jordan, Primrose Freestone
Applied and Environmental Microbiology Dec 2016, 83 (1) e02416-16; DOI: 10.1128/AEM.02416-16
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KEYWORDS

Beta vulgaris
lettuce
Plant Leaves
Salmonella enterica
Spinacia oleracea
Salmonella
fresh produce
biofilm
motility
salad leaf colonization

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