Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics

Reuterin is a dynamic small-molecule complex produced through glycerol fermentation by <i>Limosilactobacillus reuteri</i> and has potential as a food biopreservative. Despite its broad-spectrum antimicrobial activity, the underlying mechanism of action of reuterin is still elusive. The p...

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Main Authors: Mao-Cheng Sun, Dian-Dian Li, Yu-Xin Chen, Xiu-Juan Fan, Yu Gao, Haiqing Ye, Tiehua Zhang, Changhui Zhao
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Foods
Subjects:
Online Access:https://www.mdpi.com/2304-8158/12/23/4208
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author Mao-Cheng Sun
Dian-Dian Li
Yu-Xin Chen
Xiu-Juan Fan
Yu Gao
Haiqing Ye
Tiehua Zhang
Changhui Zhao
author_facet Mao-Cheng Sun
Dian-Dian Li
Yu-Xin Chen
Xiu-Juan Fan
Yu Gao
Haiqing Ye
Tiehua Zhang
Changhui Zhao
author_sort Mao-Cheng Sun
collection DOAJ
description Reuterin is a dynamic small-molecule complex produced through glycerol fermentation by <i>Limosilactobacillus reuteri</i> and has potential as a food biopreservative. Despite its broad-spectrum antimicrobial activity, the underlying mechanism of action of reuterin is still elusive. The present paper aimed to explore the antibacterial mechanism of reuterin and its effects on membrane damage and the intracellular metabolome of <i>S. aureus</i>. Our results showed that reuterin has a minimum inhibitory concentration of 18.25 mM against <i>S. aureus</i>, based on the 3-hydroxypropionaldehyde level. Key indicators such as extracellular electrical conductivity, membrane potential and permeability were significantly increased, while intracellular pH, ATP and DNA were markedly decreased, implying that reuterin causes a disruption to the structure of the cell membrane. The morphological damage to the cells was confirmed by scanning electron microscopy. Subsequent metabolomic analysis identified significant alterations in metabolites primarily involved in lipid, amino acid, carbohydrate metabolism and phosphotransferase system, which is crucial for cell membrane regulation and energy supply. Consequently, these findings indicated that the antibacterial mechanism of reuterin initially targets lipid and amino acid metabolism, leading to cell membrane damage, which subsequently results in energy metabolism disorder and, ultimately, cell death. This paper offers innovative perspectives on the antibacterial mechanism of reuterin, contributing to its potential application as a food preservative.
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spelling doaj.art-4fd055d3dafc4ea3acce0df72cc674952023-12-08T15:15:18ZengMDPI AGFoods2304-81582023-11-011223420810.3390/foods12234208Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted MetabolomicsMao-Cheng Sun0Dian-Dian Li1Yu-Xin Chen2Xiu-Juan Fan3Yu Gao4Haiqing Ye5Tiehua Zhang6Changhui Zhao7College of Food Science and Engineering, Changchun University, Changchun 130022, ChinaCollege of Food Science and Engineering, Changchun University, Changchun 130022, ChinaCollege of Food Science and Engineering, Changchun University, Changchun 130022, ChinaCollege of Food Science and Engineering, Changchun University, Changchun 130022, ChinaCollege of Food Science and Engineering, Changchun University, Changchun 130022, ChinaCollege of Food Science and Engineering, Jilin University, Changchun 130062, ChinaCollege of Food Science and Engineering, Jilin University, Changchun 130062, ChinaCollege of Food Science and Engineering, Jilin University, Changchun 130062, ChinaReuterin is a dynamic small-molecule complex produced through glycerol fermentation by <i>Limosilactobacillus reuteri</i> and has potential as a food biopreservative. Despite its broad-spectrum antimicrobial activity, the underlying mechanism of action of reuterin is still elusive. The present paper aimed to explore the antibacterial mechanism of reuterin and its effects on membrane damage and the intracellular metabolome of <i>S. aureus</i>. Our results showed that reuterin has a minimum inhibitory concentration of 18.25 mM against <i>S. aureus</i>, based on the 3-hydroxypropionaldehyde level. Key indicators such as extracellular electrical conductivity, membrane potential and permeability were significantly increased, while intracellular pH, ATP and DNA were markedly decreased, implying that reuterin causes a disruption to the structure of the cell membrane. The morphological damage to the cells was confirmed by scanning electron microscopy. Subsequent metabolomic analysis identified significant alterations in metabolites primarily involved in lipid, amino acid, carbohydrate metabolism and phosphotransferase system, which is crucial for cell membrane regulation and energy supply. Consequently, these findings indicated that the antibacterial mechanism of reuterin initially targets lipid and amino acid metabolism, leading to cell membrane damage, which subsequently results in energy metabolism disorder and, ultimately, cell death. This paper offers innovative perspectives on the antibacterial mechanism of reuterin, contributing to its potential application as a food preservative.https://www.mdpi.com/2304-8158/12/23/4208reuterin3-hydroxypropionaldehyde3-HPAfood biopreservative<i>Staphylococcus aureus</i>antibacterial mechanism
spellingShingle Mao-Cheng Sun
Dian-Dian Li
Yu-Xin Chen
Xiu-Juan Fan
Yu Gao
Haiqing Ye
Tiehua Zhang
Changhui Zhao
Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
Foods
reuterin
3-hydroxypropionaldehyde
3-HPA
food biopreservative
<i>Staphylococcus aureus</i>
antibacterial mechanism
title Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
title_full Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
title_fullStr Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
title_full_unstemmed Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
title_short Insights into the Mechanisms of Reuterin against <i>Staphylococcus aureus</i> Based on Membrane Damage and Untargeted Metabolomics
title_sort insights into the mechanisms of reuterin against i staphylococcus aureus i based on membrane damage and untargeted metabolomics
topic reuterin
3-hydroxypropionaldehyde
3-HPA
food biopreservative
<i>Staphylococcus aureus</i>
antibacterial mechanism
url https://www.mdpi.com/2304-8158/12/23/4208
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