Biocontrol of the food-borne pathogens Listeria monocytogenes and Salmonella enterica serovar Poona on fresh-cut apples with naturally occurring bacterial and yeast antagonists

Abstract

Fresh-cut apples contaminated with either Listeria monocytogenes or Salmonella enterica serovar Poona, using strains implicated in outbreaks, were treated with one of 17 antagonists originally selected for their ability to inhibit fungal postharvest decay on fruit. While most of the antagonists increased the growth of the food-borne pathogens, four of them, including Gluconobacter asaii (T1-D1), a Candida sp. (T4-E4), Discosphaerina fagi (ST1-C9), and Metschnikowia pulcherrima (T1-E2), proved effective in preventing the growth or survival of food-borne human pathogens on fresh-cut apple tissue. The contaminated apple tissue plugs were stored for up to 7 days at two different temperatures. The four antagonists survived or grew on the apple tissue at 10 or 25 degrees C. These four antagonists reduced the Listeria monocytogenes populations and except for the Candida sp. (T4-E4), also reduced the S. enterica serovar Poona populations. The reduction was higher at 25 degrees C than at 10 degrees C, and the growth of the antagonists, as well as pathogens, increased at the higher temperature.

FIG. 1.

Interaction means of populations of Listeria monocytogenes in the presence of four different antagonists on Golden Delicious apple plugs stored at 10°C over 7 days. In the table, treatment means within columns with different letters (a, b) and time means within rows with different letters (x, y, z) are significantly different at the 0.05 level. Log CFU values were initially analyzed as a three-factor general linear mixed model with treatment and time as the fixed factors and experiment the random block factor. Experiment was not included in the final analysis because it accounted for little variability. Variance grouping was used. Means and mean comparisons are given.

FIG. 2.

Interaction means of populations of Listeria monocytogenes in the presence of four different antagonists on Golden Delicious apple plugs stored at 25°C over 7 days. Table footnotes: 1 and 2, treatment means within columns with different letters (a, b) and time means within rows with different letters (y, z) are significantly different at the 0.05 level; 3, treatment mean not different from zero at P < 0.05. Treatments with at least one nonzero CFU value were analyzed as a one-factor general linear model with Listeria-time coded as treatment. To correct for variance heterogeneity the variance grouping technique was used. The result was statistically significant (F = 1,186,70, P < 0.0001, df = 13). As treatment was statistically significant, mean comparisons are given.

FIG. 3.

Interaction means of populations of Salmonella Poona in the presence of three different antagonists on Golden Delicious apple plugs stored at 25° over 7 days. In the table, treatment means within columns with different letters (a, b) and time means within rows with different letters (x, y, z) are significantly different at the 0.05 level. The treatment × storage time means with all nonzero log CFU values were analyzed as a three-factor general linear mixed model with treatment and storage time as the fixed factors and experiment as the random block factor. As experiment accounted for little variability, about 2% of the residual, all treatment × storage time values were used in a two-factor general linear model for treatment and storage time. To correct for variance heterogeneity the variance grouping technique was used. Means and mean comparisons are given. As the treatment × storage time interaction was statistically significant, mean comparisons are given.

FIG. 4.

Interaction means of populations of antagonists in the presence of either S. enterica serovar Poona or L. monocytogenes from Golden Delicious apple plugs stored at 10 or 25°C over 7 days. The recovered antagonist populations were analyzed separately. As experiment accounted for very little variability, about 1% of the residual, the values were modeled as a two-factor model. To correct for variance heterogeneity the variance grouping technique was used. As time was statistically significant the mean comparisons are indicated with different letters (significant at P < 0.05). There was no difference between the growth of the antagonists. The difference over time was significant and was calculated from the means at 10 and 25°C combined.