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; KARAMPUDI, 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., Karampudi, 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: Chlorine dioxide gas is emerging as a potent treatment for the control of microorganisms on fresh produce in a post-harvest setting. However, the mechanisms behind how bacteria respond to treatment are poorly understood. The purpose of this study was to examine responses to gaseous chlorine dioxide by Escherichia coli O157:H7 at the transcriptome level to better understand the gene-regulation employed by bacteria to defend against treatment and develop treatment-resistance. Between the first hour and second hour of treatment, primary defense and survival genes shifted from consistent upregulation to substantial downregulation, indicating that maximum treatment effectiveness is reached during the first hour and adaptation could be occurring after two hours of treatment. These results highlight at what exposure treatment is effective and the risks of development of treatment-resistance due to over-exposure.

Technical Abstract: The enteropathogenic Shiga toxin-producing Escherichia coli (STEC) perennially causes of poisoning from fresh fruits and vegetables. While treatment with gaseous ClO2 has been exposure as a potent intervention strategy particularly on fresh tomato, not much is known about the nature of its xenobiotic effects and the dynamics of bacterial responses to sub-optimal, optimal, and supraoptimal exposure. This study examined the temporal transcriptome of STEC during exposure to exogenous ClO2 in order to elucidate the genetic mechanisms employed by the pathogen for defenses, and the understand the risks of potential adaptation. A dose of 1 µg ClO2 per gram of tomato fruits induced different effects depending on exposure time. First hour exposure caused only partial killing with the transcriptional networks reflecting the activation of primary defense and survival mechanisms via the two component system, pathogenesis and virulence, secretory system, nutrient reallocation towards stress responses, prophage induction, quorum sensing, surface attachment, and biofilm formation. Defense response was attenuated with massive bacterial cell death during the second and third hours. Transcriptional networks during the second hour optimal killing phase was characterized by massive downregulation of primary defenses that spiked during the first hour, indicating that the potency of xenobiotic effects had surpassed the maximum defense potential of the pathogen. While there was no further increase in bacteria death during the third hour, the transcriptional network included a second burst of defense response that appeared the be independent of the primary defenses during the first hour, suggestive of potential adaptation.