Xenobiotic Effects of Chlorine Dioxide to Escherichia coli O157:H7 on Non-host Tomato Environment Revealed by Transcriptional Network Modeling: Implications to Adaptation and Selection

Escherichia coli serotype O157:H7 is one of the major agents of pathogen outbreaks associated with fresh fruits and vegetables. Gaseous chlorine dioxide (ClO(2)) has been reported to be an effective intervention to eliminate bacterial contamination on fresh produce. Although remarkable positive effects of low doses of ClO(2) 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 ClO(2) in order to elucidate the genetic mechanisms underlying bacterial survival under such harsh conditions. Dosages of 1 μg, 5 μg, and 10 μg ClO(2) per gram of tomato fruits cause different effects with dose-by-time dynamics. The first hour of exposure to 1 μg and 5 μg ClO(2) 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 ClO(2) 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 ClO(2) 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 ClO(2), 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 ClO(2) 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 ClO(2), 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.