Food Control 125 (2021) 107974
Available online 12 February 2021
0956-7135/© 2021 Elsevier Ltd. All rights reserved.
NMR-based metabolomic investigation of antimicrobial mechanism of
electrolysed water combined with moderate heat treatment against Listeria
monocytogenes on salmon
Jiaying Wu
a, b
, Lin Zhao
a, b
, Shaojuan Lai
c, d
, Hongshun Yang
a, b, *
a
Department of Food Science and Technology, National University of Singapore, Singapore, 117542, Singapore
b
National University of Singapore (Suzhou) Research Institute, 377 Lin Quan Street, Suzhou Industrial Park, Suzhou, Jiangsu, 215123, PR China
c
College of Basic Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou, 550025, PR China
d
Guangzhou Pulu Medical Technology Co., Ltd, Guangzhou, Guangdong, 510800, PR China
A R T I C L E INFO
Keywords:
Heat
Oxidative stress
Foodborne pathogen
Foodomics
Electrolyzed water
ABSTRACT
Heat and acidic electrolysed water (AEW) are considered effective for inactivation of microorganisms. While a
previous study elucidated their bactericidal mechanism on Listeria innocua through metabolomics in vitro, the
fundamental mechanism for inaction of L. monocytogenes using this method in food system is poorly understood.
This work determined the survival population and injury of three L. monocytogenes strains (SSA81, LM44, and
LM3) inoculated on salmon under heat (60
◦
C) and AEW (100 mg/L available free chlorine, pH 2.42, oxidation
reduction potential 1182 mV) treatments, when applied alone or in combination. The bactericidal mechanism
was explored by utilising nuclear magnetic resonance (NMR) and multivariate data analysis. Our results indi-
cated that the individual heat and AEW treatment led to 0.4 and 1.2 log CFU/g reductions of L. monocytogenes,
respectively. The combined treatment of heat and AEW resulted in notable reductions which were 2.1–2.2 log
CFU/g for L. monocytogenes. More than 25%, 35%, and 55% injury of L. monocytogenes were observed under heat,
AEW, and the combined treatment, respectively. Overall, 43 metabolites were characterised in three strains.
Short time heat might activate protective system of the cells by accumulating amino acids and organic acids.
AEW resulted in the reductions of metabolites due to oxidative and acid stress. In the combined treatment, AEW
played the main role and its bactericidal ability was strengthened by heat. Signifcant decreases of Val, Leu, Tyr,
and Trp were detected in all strains under the synergic stress of heat and AEW (P < 0.05). There were 15, 7, and 6
pathways, mainly included amino acid, energy, and carbohydrate metabolisms, changed signifcantly under the
combined treatment for SSA81, LM44, and LM3, respectively. The strain LM3 presented the strongest resistance
to oxidative stress by the enhancement of Glu decarboxylase system, whereas this compensatory pathway was
diminished in SSA81 and LM44. These fndings suggest that the bactericidal mechanism can be well explained by
disturbed pathways.
1. Introduction
Listeriosis is a potentially fatal foodborne illness caused by Listeria
monocytogenes, a Gram-positive pathogenic bacterium. The Centers for
Disease Control and Prevention (CDC) estimated that in the United
States, almost 1600 people suffer from listeriosis every year, leading to
260 deaths. Due to the high mortality rate, government and food safety
organisations have implemented serious surveillance and monitoring
system (Todd & Notermans, 2011). It has been widely recognised that
ready-to-eat (RTE) foods can be contaminated by L. monocytogenes. Its
presence has been reported in smoked salmon (Josewin et al., 2018),
cheese (Park & Ha, 2020), and salads (Lokerse et al., 2016). The strong
survival abilities under extremely adverse environments, such as high
temperature, low water activities, and acidic pH, make its control
challenging (Wang & Shen, 2015).
Salmon is a potential source of contamination and a favourable
substrate of L. monocytogenes, although the “zero-tolerance” policy,
which means no detection of L. monocytogenes in either two of the 25 g
samples tested, has been established by both Food and Drug Adminis-
tration (FDA) and Food Safety and Inspection Services (FSIS) (Huang,
* Corresponding author. Department of Food Science and Technology, National University of Singapore, Singapore, 117542, Singapore.
E-mail address: fstynghs@nus.edu.sg (H. Yang).
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Food Control
journal homepage: www.elsevier.com/locate/foodcont
https://doi.org/10.1016/j.foodcont.2021.107974
Received 24 October 2020; Received in revised form 5 February 2021; Accepted 7 February 2021