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

Authors: SHU, XIAOMEI - Texas Tech University; SINGH, MANAVI - Texas Tech University; BHUSHANA, NAGA - Texas Tech University; Bridges, David; KITAZUMI, AI - Texas Tech University; Wu, Vivian; DE LOS REYES, BENILDO - Texas Tech University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2020
Publication Date: 6/3/2020
Citation: Shu, X., Singh, M., Bhushana, N.B., Bridges, D.F., Kitazumi, A., Wu, V.C., De Los Reyes, B.G. 2020. 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. Frontiers in Microbiology. 11:1122. https://doi.org/10.3389/fmicb.2020.01122.
DOI: https://doi.org/10.3389/fmicb.2020.01122

Interpretive Summary: Escherichia coli is a food borne human pathogen which can cause outbreaks via contaminated fresh tomato fruits. The Shiga toxin-producing E. coli serotype O157:H7 causes hemorrhagic colitis and hemolytic uremic syndrome once a patient has been infected by the pathogen through consuming contaminated food. Bridges et al. (2018) reported that gaseous chlorine dioxide (ClO2) is an effective intervention to decontaminate E. coli on fresh produce. Shu et al. (in press) analyzed the gene co-expression networks in E. coli exposed to low dose of ClO2. However, the genetic and molecular mechanisms of how E. coli respond to high doses of ClO2 treatment remain unclear. In this study, we examined the temporal gene co-expression networks of E. coli O157:H7 during exposure to two different high doses of ClO2. We found that the potency of xenobiotic effects high dose of ClO2 with longer exposure time induced potential adaptation in the bacteria. We generated critical knowledge in investigation of optimal chemical intervention on fresh tomato fruits without introducing potential risks of adaptation. We also established a novel gene co-expression networking method that could be used as a powerful tool to investigate the molecular and genetic mechanisms underlying the response of microorganisms to various environmental stimuli.

Technical Abstract: Escherichia coli serotype O157:H7 is one of the major causing agents of outbreaks associated with fresh fruits and vegetables. Gaseous chlorine dioxide (ClO2) has been reported to be an effective intervention to eliminate bacteria on fresh produce. Although a remarkable scenario was reported in E. coli exposed to low dose of ClO2, regulatory mechanisms coordinating high doses of ClO2 exposure and potential bacterial adaptation remind unclear. This study examined the temporal transcriptome of E. coli O157:H7 during exposure to high doses of ClO2 in order to elucidate the genetic mechanisms of how E. coli survive under these harsh environmental conditions. Two doses of 5 and 10 µg ClO2 per gram of tomato fruits cause different effects depending on dose and exposure time. First hour of 5 µg ClO2 exposure caused only partial killing, with significant growth reduction starting at the second hour, while without further significant growth reduction at third hour. However, 10 µg ClO2 exposure led to massive bacterial cell death at 1 hour, with further increased cell death at 2 and 3 hours. Upon 5 µg ClO2 treatment, transcriptional networks showed massive downregulation of pathogenesis and stress response genes at the first hour of exposure, with the number of differentially expressed genes to be decreased at the second and third hours. Defense was attenuated with significant growth reduction during the second and third hours. In contrast, more genes were downregulated when the bacteria were exposed to 10 µg ClO2 at the first hour, with the number of both up and downregulated genes to be decreased at the second hour. However, a total of 810 genes were uniquely upregulated at the third hour when the bacteria were treated with 10 µg ClO2, suggesting that the potency of xenobiotic effects had led to potential adaptation. This study provided important knowledge in selection of target molecules for eliminating the bacterial contamination in fresh produce without overlooking potential risks of adaptation.