The role of PhoP/PhoQ system in regulating stress adaptation response in Escherichia coli O157:H7

Jina Han; Xu Gao; Xin Luo; Lixian Zhu; Yimin Zhang; Pengcheng Dong

doi:10.1016/j.fm.2023.104244

The role of PhoP/PhoQ system in regulating stress adaptation response in Escherichia coli O157:H7

Food Microbiol. 2023 Jun:112:104244. doi: 10.1016/j.fm.2023.104244. Epub 2023 Feb 22.

Authors

Jina Han¹, Xu Gao¹, Xin Luo¹, Lixian Zhu¹, Yimin Zhang², Pengcheng Dong³

Affiliations

¹ Lab of Beef Processing and Quality Control, College of Food Science and Engineering, Shandong Agricultural University, Tai'an, Shandong, 271018, PR China; National R&D Center for Beef Processing Technology, Tai'an, Shandong, 271018, PR China.
² Lab of Beef Processing and Quality Control, College of Food Science and Engineering, Shandong Agricultural University, Tai'an, Shandong, 271018, PR China; National R&D Center for Beef Processing Technology, Tai'an, Shandong, 271018, PR China. Electronic address: ymzhang@sdau.edu.cn.
³ Lab of Beef Processing and Quality Control, College of Food Science and Engineering, Shandong Agricultural University, Tai'an, Shandong, 271018, PR China; National R&D Center for Beef Processing Technology, Tai'an, Shandong, 271018, PR China. Electronic address: pcdong@sdau.edu.cn.

PMID: 36906298
DOI: 10.1016/j.fm.2023.104244

Abstract

The development of acid tolerance response (ATR) as a result of low pH in Escherichia coli O157:H7 (E. coli O157:H7) contaminating beef during processing is considered a major food safety concern. Thus, in order to explore the formation and molecular mechanisms of the tolerance response of E. coli O157:H7 in a simulated beef processing environment, the resistance of a wild-type (WT) strain and its corresponding ΔphoP mutant to acid, heat, and osmotic pressure was evaluated. Strains were pre-adapted under different conditions of pH (5.4 and 7.0), temperature (37 °C and 10 °C), and culture medium (meat extract and Luria-Bertani broth media). In addition, the expression of genes related to stress response and virulence was also investigated among WT and ΔphoP strains under the tested conditions. Pre-acid adaptation increased the resistance of E. coli O157:H7 to acid and heat treatment while resistance to osmotic pressure decreased. Moreover, acid adaptation in meat extract medium simulating slaughter environment increased ATR, whereas pre-adaptation at 10 °C reduced the ATR. Furthermore, it was shown that mildly acidic conditions (pH = 5.4) and the PhoP/PhoQ two-component system (TCS) acted synergistically to enhance acid and heat tolerance in E. coli O157:H7. Additionally, the expression of genes related to arginine and lysine metabolism, heat shock, and invasiveness was up-regulated, which revealed that the mechanism of acid resistance and cross-protection under mildly acidic conditions was mediated by the PhoP/PhoQ TCS. Both acid adaptation and phoP gene knockout reduced the relative expression of stx1 and stx2 genes which were considered as critical pathogenic factors. Collectively, the current findings indicated that ATR could occur in E. coli O157:H7 during beef processing. Thus, there is an increased food safety risk due to the persistence of tolerance response in the following processing conditions. The present study provides a more comprehensive basis for the effective application of hurdle technology in beef processing.

Keywords: Acid tolerance response; Arginine decarboxylase; Cross-protection; Escherichia coli; Meat extract; Two component regulatory system.

MeSH terms

Adaptation, Physiological
Animals
Cattle
Colony Count, Microbial
Escherichia coli O157*
Escherichia coli Proteins*
Food Contamination / analysis
Food Handling
Food Microbiology
Hydrogen-Ion Concentration
Meat

Substances

PhoP protein, E coli
Escherichia coli Proteins