The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt

ABSTRACT: In this study, the effect of luxS, a key gene involved in quorum sensing, on the characteristic flavor of yogurt and its molecular mechanisms during the cofermentation of yogurt with engineered probiotics was investigated. The luxS gene overexpression strain was constructed by the homologo...

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Main Authors: Ruitong Zhang, Zihang Shi, Xiankang Fan, Tao Zhang, Maolin Tu, Zhen Wu, Xiaoqun Zeng, Weichen Bao, Bo Chen, Daodong Pan
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Journal of Dairy Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0022030225002103
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author Ruitong Zhang
Zihang Shi
Xiankang Fan
Tao Zhang
Maolin Tu
Zhen Wu
Xiaoqun Zeng
Weichen Bao
Bo Chen
Daodong Pan
author_facet Ruitong Zhang
Zihang Shi
Xiankang Fan
Tao Zhang
Maolin Tu
Zhen Wu
Xiaoqun Zeng
Weichen Bao
Bo Chen
Daodong Pan
author_sort Ruitong Zhang
collection DOAJ
description ABSTRACT: In this study, the effect of luxS, a key gene involved in quorum sensing, on the characteristic flavor of yogurt and its molecular mechanisms during the cofermentation of yogurt with engineered probiotics was investigated. The luxS gene overexpression strain was constructed by the homologous recombination technique, and its effect on the expression of population sensing signaling molecules and luxS gene was determined by bioluminescence and quantitative real-time PCR, and finally, headspace solid-phase micro extraction-GC-MS (HS-SPME-GC-MS) and metabolomics were used to determine the mechanism of its effect on the characteristic flavor of yogurt. The results demonstrated that the overexpression strains of Lactobacillus acidophilus CICC 6074-pMG36e-luxS and Lactobacillus helveticus R0052-pMG36e-luxS were successfully constructed. The expression of the luxS gene was upregulated by 2.25-fold and 3.16-fold, respectively. Compared with the wild-type strains, yogurt fermented by the overexpression strains showed a significant increase in AI-2 content, acidity, viable bacterial count, and protein hydrolysis, whereas pH, water-holding capacity, and hardness were significantly reduced. The HS-SPME-GC-MS results revealed the presence of 31 volatile flavor substances in yogurt. Among them, benzaldehyde (almond and burned sugar flavors), 2,4-dimethyl- (almond, cherry, and naphthalene flavors), dibutyl phthalate (a faint aromatic odor), and n-decanoic acid (rancid and fatty notes) were identified as the key differential flavor substances mediated by the luxS gene. Metabolomics results showed that the luxS gene mediates the production of organic acids in yogurt through arginine and proline metabolism, phenylalanine metabolism, and tryptophan metabolism. This study provides a theoretical basis for a deeper understanding of the molecular mechanisms underlying yogurt flavor formation.
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spelling doaj-art-0372d05dcc104a418dda59f18b7d04a52025-08-20T01:48:20ZengElsevierJournal of Dairy Science0022-03022025-05-0110854734474810.3168/jds.2025-26323The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurtRuitong Zhang0Zihang Shi1Xiankang Fan2Tao Zhang3Maolin Tu4Zhen Wu5Xiaoqun Zeng6Weichen Bao7Bo Chen8Daodong Pan9State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, ChinaCollege of Food Science and Technology, Hunan Agricultural University, Changsha 410114, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Corresponding authorsState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, ChinaJinhua Yinhe Biological Technology Co. Ltd., Jinhua 321000, ChinaZhejiang Yiming Food Co. Ltd., Zhejiang 325400, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, College of Food Science and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China; Key Laboratory for Food Microbiology and Nutrition of Zhejiang Province, Ningbo University, Ningbo 315211, China; Corresponding authorsABSTRACT: In this study, the effect of luxS, a key gene involved in quorum sensing, on the characteristic flavor of yogurt and its molecular mechanisms during the cofermentation of yogurt with engineered probiotics was investigated. The luxS gene overexpression strain was constructed by the homologous recombination technique, and its effect on the expression of population sensing signaling molecules and luxS gene was determined by bioluminescence and quantitative real-time PCR, and finally, headspace solid-phase micro extraction-GC-MS (HS-SPME-GC-MS) and metabolomics were used to determine the mechanism of its effect on the characteristic flavor of yogurt. The results demonstrated that the overexpression strains of Lactobacillus acidophilus CICC 6074-pMG36e-luxS and Lactobacillus helveticus R0052-pMG36e-luxS were successfully constructed. The expression of the luxS gene was upregulated by 2.25-fold and 3.16-fold, respectively. Compared with the wild-type strains, yogurt fermented by the overexpression strains showed a significant increase in AI-2 content, acidity, viable bacterial count, and protein hydrolysis, whereas pH, water-holding capacity, and hardness were significantly reduced. The HS-SPME-GC-MS results revealed the presence of 31 volatile flavor substances in yogurt. Among them, benzaldehyde (almond and burned sugar flavors), 2,4-dimethyl- (almond, cherry, and naphthalene flavors), dibutyl phthalate (a faint aromatic odor), and n-decanoic acid (rancid and fatty notes) were identified as the key differential flavor substances mediated by the luxS gene. Metabolomics results showed that the luxS gene mediates the production of organic acids in yogurt through arginine and proline metabolism, phenylalanine metabolism, and tryptophan metabolism. This study provides a theoretical basis for a deeper understanding of the molecular mechanisms underlying yogurt flavor formation.http://www.sciencedirect.com/science/article/pii/S0022030225002103lactic acid bacteriaquorum sensingsignaling molecule AI-2metabolomics
spellingShingle Ruitong Zhang
Zihang Shi
Xiankang Fan
Tao Zhang
Maolin Tu
Zhen Wu
Xiaoqun Zeng
Weichen Bao
Bo Chen
Daodong Pan
The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
Journal of Dairy Science
lactic acid bacteria
quorum sensing
signaling molecule AI-2
metabolomics
title The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
title_full The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
title_fullStr The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
title_full_unstemmed The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
title_short The key quorum sensing gene luxS in Lactobacillus acidophilus CICC 6074 and Lactobacillus helveticus R0052 mediates organic acid production and promotes protein hydrolysis in yogurt
title_sort key quorum sensing gene luxs in lactobacillus acidophilus cicc 6074 and lactobacillus helveticus r0052 mediates organic acid production and promotes protein hydrolysis in yogurt
topic lactic acid bacteria
quorum sensing
signaling molecule AI-2
metabolomics
url http://www.sciencedirect.com/science/article/pii/S0022030225002103
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