Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis

Two-component systems (TCS) of <i>Salmonella enterica</i> serovar Enteritidis are composed of a histidine kinase and a response regulator (RR) and represent a critical mechanism by which bacteria develop resistance to environmental stress. Here, we characterized the functions of RRs in T...

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Main Authors: Mengjun Hu, Zhuoan Zhou, Chenqi Liu, Zeqiang Zhan, Yan Cui, Shoukui He, Xianming Shi
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Foods
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Online Access:https://www.mdpi.com/2304-8158/13/22/3709
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author Mengjun Hu
Zhuoan Zhou
Chenqi Liu
Zeqiang Zhan
Yan Cui
Shoukui He
Xianming Shi
author_facet Mengjun Hu
Zhuoan Zhou
Chenqi Liu
Zeqiang Zhan
Yan Cui
Shoukui He
Xianming Shi
author_sort Mengjun Hu
collection DOAJ
description Two-component systems (TCS) of <i>Salmonella enterica</i> serovar Enteritidis are composed of a histidine kinase and a response regulator (RR) and represent a critical mechanism by which bacteria develop resistance to environmental stress. Here, we characterized the functions of RRs in TCS in the formation of stress tolerance, motility and biofilm using twenty-six <i>S</i>. Enteritidis RR-encoding gene deletion mutants. The viability results unraveled their essential roles in resistance to elevated temperature (GlrR), pH alterations (GlrR, TctD, YedW, ArcA and YehT), high salt (PhoB, BaeR, CpxR, PhoP, UvrY and TctD), oxidative stress (PhoB, YedW, BaeR, ArcA, PhoP, UvrY, PgtA and QseB) and motility (ArcA, GlnG, PgtA, PhoB, UhpA, OmpR, UvrY and QseB) of <i>S</i>. Enteritidis. The results of the crystal violet staining, microscopy observation and Congo red binding assays demonstrated that the absence of ArcA, GlnG, PhoP, OmpR, ZraR or SsrB in <i>S</i>. Enteritidis led to a reduction in biofilms and an impairment in red/dry/rough macrocolony formation, whereas the absence of UvrY exhibited an increase in biofilms and formed a brown/smooth/sticky macrocolony. The results indicated the regulatory effects of these RRs on the production of biofilm matrix, curli fimbriae and cellulose. Our findings yielded insights into the role of TCSs, making them a promising target for combating <i>S</i>. Enteritidis.
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spelling doaj-art-a0780a4f4cc542b08dad4d607eb2962f2025-08-20T01:53:48ZengMDPI AGFoods2304-81582024-11-011322370910.3390/foods13223709Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> EnteritidisMengjun Hu0Zhuoan Zhou1Chenqi Liu2Zeqiang Zhan3Yan Cui4Shoukui He5Xianming Shi6MOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMOST-USDA Joint Research Center for Food Safety, State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaTwo-component systems (TCS) of <i>Salmonella enterica</i> serovar Enteritidis are composed of a histidine kinase and a response regulator (RR) and represent a critical mechanism by which bacteria develop resistance to environmental stress. Here, we characterized the functions of RRs in TCS in the formation of stress tolerance, motility and biofilm using twenty-six <i>S</i>. Enteritidis RR-encoding gene deletion mutants. The viability results unraveled their essential roles in resistance to elevated temperature (GlrR), pH alterations (GlrR, TctD, YedW, ArcA and YehT), high salt (PhoB, BaeR, CpxR, PhoP, UvrY and TctD), oxidative stress (PhoB, YedW, BaeR, ArcA, PhoP, UvrY, PgtA and QseB) and motility (ArcA, GlnG, PgtA, PhoB, UhpA, OmpR, UvrY and QseB) of <i>S</i>. Enteritidis. The results of the crystal violet staining, microscopy observation and Congo red binding assays demonstrated that the absence of ArcA, GlnG, PhoP, OmpR, ZraR or SsrB in <i>S</i>. Enteritidis led to a reduction in biofilms and an impairment in red/dry/rough macrocolony formation, whereas the absence of UvrY exhibited an increase in biofilms and formed a brown/smooth/sticky macrocolony. The results indicated the regulatory effects of these RRs on the production of biofilm matrix, curli fimbriae and cellulose. Our findings yielded insights into the role of TCSs, making them a promising target for combating <i>S</i>. Enteritidis.https://www.mdpi.com/2304-8158/13/22/3709<i>S</i>. EnteritidisTCSresponse regulatorenvironmental stressbiofilm matrix
spellingShingle Mengjun Hu
Zhuoan Zhou
Chenqi Liu
Zeqiang Zhan
Yan Cui
Shoukui He
Xianming Shi
Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
Foods
<i>S</i>. Enteritidis
TCS
response regulator
environmental stress
biofilm matrix
title Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
title_full Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
title_fullStr Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
title_full_unstemmed Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
title_short Roles of Response Regulators in the Two-Component System in the Formation of Stress Tolerance, Motility and Biofilm in <i>Salmonella</i> Enteritidis
title_sort roles of response regulators in the two component system in the formation of stress tolerance motility and biofilm in i salmonella i enteritidis
topic <i>S</i>. Enteritidis
TCS
response regulator
environmental stress
biofilm matrix
url https://www.mdpi.com/2304-8158/13/22/3709
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