Abstract
Escherichia coli serotype O157:H7 is one of the major agents of pathogen outbreaks associated with fresh fruits and vegetables. Gaseous chlorine dioxide (ClO2) has been reported to be an effective intervention to eliminate bacterial contamination on fresh produce. Although remarkable positive effects of low doses of ClO2 have been reported, the genetic regulatory machinery coordinating the mechanisms of xenobiotic effects and the potential bacterial adaptation remained unclear. This study examined the temporal transcriptome profiles of E. coli O157:H7 during exposure to different doses of ClO2 in order to elucidate the genetic mechanisms underlying bacterial survival under such harsh conditions. Dosages of 1 μg, 5 μg, and 10 μg ClO2 per gram of tomato fruits cause different effects with dose-by-time dynamics. The first hour of exposure to 1 μg and 5 μg ClO2 caused only partial killing with significant growth reduction starting at the second hour, and without further significant reduction at the third hour. However, 10 μg ClO2 exposure led to massive bacterial cell death at 1 h with further increase in cell death at 2 and 3 h. The first hour exposure to 1 μg ClO2 caused activation of primary defense and survival mechanisms. However, the defense response was attenuated during the second and third hours. Upon treatment with 5 μg ClO2, the transcriptional networks showed massive downregulation of pathogenesis and stress response genes at the first hour of exposure, with decreasing number of differentially expressed genes at the second and third hours. In contrast, more genes were further downregulated with exposure to 10 μg ClO2 at the first hour, with the number of both upregulated and downregulated genes significantly decreasing at the second hour. A total of 810 genes were uniquely upregulated at the third hour at 10 μg ClO2, suggesting that the potency of xenobiotic effects had led to potential adaptation. This study provides important knowledge on the possible selection of target molecules for eliminating bacterial contamination on fresh produce without overlooking potential risks of adaptation.
Highlights
Illnesses caused by the foodborne enteropathogen and Shiga toxin-producing Escherichia coli O157 (STEC) can be lifethreatening (Nataro and Kaper, 1998; Law, 2001; Santiago et al, 2017)
In order to understand the impact of xenobiotic effects of different ClO2 dosage, and exposure time on bacterial viability and regrowth ability, and the potential impact of prolonged time to potential supra-optimal effects, we assessed the survival of E. coli O157:H7 on the surface of tomato produce at three different dosages of gaseous ClO2 (1, 5, and 10 μg per grams of ripen fruits) at room temperature
Since optimizing dosage and exposure time to the xenobiotic agent are of primary importance as a means of preserving the integrity and quality of the produce, our data implied that exposure to 10 μg ClO2 resulted in similar effects on bacterial killing, a higher dosage with shorter exposure time is adequate for optimal effect
Summary
Illnesses caused by the foodborne enteropathogen and Shiga toxin-producing Escherichia coli O157 (STEC) can be lifethreatening (Nataro and Kaper, 1998; Law, 2001; Santiago et al, 2017). Most of the STEC strains identified by USDA carry toxin genes stx1a and stx2a (González-Escalona and Kase, 2019). E. coli serotype O157:H7 has been reported to be the source of outbreaks on fresh produce such as tomato fruits (Solanum lycopersicum L.) (Gomez-Aldapa et al, 2013). It has been reported that STEC contamination of non-host tomato occurred at different developmental stages through various routes (Hwang et al, 2017; Bridges et al, 2018). STEC is capable of contaminating tomato with significant wounding, which provides enormous inocula that can cause cross-contamination during subsequent post-harvest processing and transportation (Yeni et al, 2016; Cai et al, 2018)
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