{"title":"Characterization and immunoprotection of thioredoxin reductase TrxB knockout mutant of <i>Salmonella</i> Enteritidis.","authors":"Siping Zhu, Lili Wang, Hong Li, Chihuan Li, Xintong Zhu, Chao Ren, Xiaochen Liu, Yulai Dong, Qiumei Shi, Zhiqiang Zhang","doi":"10.3389/fcimb.2025.1659729","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong><i>Salmonella</i> Enteritidis (<i>S</i>. Enteritidis) is an important zoonotic pathogen that poses a major threat to animals and human health. TrxB, as a key component of the thioredoxin system, is a thioredoxin reductase ubiquitously present in organisms. It is mainly involved in maintaining cellular redox balance, but its role in the pathogenicity of <i>S</i>. Enteritidis remains unclear.</p><p><strong>Methods: </strong>In this study, we generated a <i>trxB</i>-deficient strain from <i>S</i>. Enteritidis C50336 strain to investigate how TrxB affects the biological characteristics and pathogenesis of the bacterium. The virulence of Δ<i>trxB</i> was assessed by measuring Δ<i>trxB</i> resistance to environmental stress, biofilm formation ability, motility, adhesion, invasion ability, intracellular survival, LD<sub>50</sub>, virulence gene expression levels, and <i>in vivo</i> colonization ability. Additionally, the study measured specific IgG antibody levels in mice, lymphocyte proliferation, and the immunoprotective effect of Δ<i>trxB</i>.</p><p><strong>Results: </strong>We found that deletion of <i>trxB</i> gene did not affect the growth and biochemical properties of the <i>S</i>. Enteritidis strain but significantly reduced its motility, drug resistance, biofilm formation, and tolerance to environmental stress. After <i>trxB</i> knocked out, the adhesion and invasion capacities of <i>S</i>. Enteritidis to Caco-2 cells, along with its proliferation in RAW264.7 cells, were significantly reduced. Additionally, the <i>trxB</i>-deficient strain exhibited significantly lower pathogenicity than the parental strain, evidenced by a more than 100-fold increase in LD<sub>50</sub>. We also observed a significant decrease in the expression of virulence-related genes in the <i>trxB</i>-knockout mutant. More importantly, immunization with this deletion strain can confer promising protection against challenge with the C50336 strain.</p><p><strong>Conclusion: </strong>These findings indicate that TrxB is a crucial virulence factor in <i>S</i>. Enteritidis, playing critical roles in its pathogenicity.</p>","PeriodicalId":12458,"journal":{"name":"Frontiers in Cellular and Infection Microbiology","volume":"15 ","pages":"1659729"},"PeriodicalIF":4.8000,"publicationDate":"2025-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12484166/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Cellular and Infection Microbiology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3389/fcimb.2025.1659729","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"IMMUNOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Salmonella Enteritidis (S. Enteritidis) is an important zoonotic pathogen that poses a major threat to animals and human health. TrxB, as a key component of the thioredoxin system, is a thioredoxin reductase ubiquitously present in organisms. It is mainly involved in maintaining cellular redox balance, but its role in the pathogenicity of S. Enteritidis remains unclear.
Methods: In this study, we generated a trxB-deficient strain from S. Enteritidis C50336 strain to investigate how TrxB affects the biological characteristics and pathogenesis of the bacterium. The virulence of ΔtrxB was assessed by measuring ΔtrxB resistance to environmental stress, biofilm formation ability, motility, adhesion, invasion ability, intracellular survival, LD50, virulence gene expression levels, and in vivo colonization ability. Additionally, the study measured specific IgG antibody levels in mice, lymphocyte proliferation, and the immunoprotective effect of ΔtrxB.
Results: We found that deletion of trxB gene did not affect the growth and biochemical properties of the S. Enteritidis strain but significantly reduced its motility, drug resistance, biofilm formation, and tolerance to environmental stress. After trxB knocked out, the adhesion and invasion capacities of S. Enteritidis to Caco-2 cells, along with its proliferation in RAW264.7 cells, were significantly reduced. Additionally, the trxB-deficient strain exhibited significantly lower pathogenicity than the parental strain, evidenced by a more than 100-fold increase in LD50. We also observed a significant decrease in the expression of virulence-related genes in the trxB-knockout mutant. More importantly, immunization with this deletion strain can confer promising protection against challenge with the C50336 strain.
Conclusion: These findings indicate that TrxB is a crucial virulence factor in S. Enteritidis, playing critical roles in its pathogenicity.
期刊介绍：
Frontiers in Cellular and Infection Microbiology is a leading specialty journal, publishing rigorously peer-reviewed research across all pathogenic microorganisms and their interaction with their hosts. Chief Editor Yousef Abu Kwaik, University of Louisville is supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide.
Frontiers in Cellular and Infection Microbiology includes research on bacteria, fungi, parasites, viruses, endosymbionts, prions and all microbial pathogens as well as the microbiota and its effect on health and disease in various hosts. The research approaches include molecular microbiology, cellular microbiology, gene regulation, proteomics, signal transduction, pathogenic evolution, genomics, structural biology, and virulence factors as well as model hosts. Areas of research to counteract infectious agents by the host include the host innate and adaptive immune responses as well as metabolic restrictions to various pathogenic microorganisms, vaccine design and development against various pathogenic microorganisms, and the mechanisms of antibiotic resistance and its countermeasures.
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