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Article(id=1192149547934695511, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250168, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1740931200000, receivedDateStr=2025-03-03, revisedDate=null, revisedDateStr=null, acceptedDate=1746979200000, acceptedDateStr=2025-05-12, onlineDate=1762160201295, onlineDateStr=2025-11-03, pubDate=1756915200000, pubDateStr=2025-09-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1762160201295, onlineIssueDateStr=2025-11-03, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1762160201295, creator=13701087609, updateTime=1762160201295, updator=13701087609, issue=Issue{id=1192149543010582589, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='10', pageStart='4241', pageEnd='4713', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1762160200113, creator=13701087609, updateTime=1762160638682, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1192151382586175735, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1192151382586175736, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=4420, endPage=4430, ext={EN=ArticleExt(id=1192149548161187930, articleId=1192149547934695511, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Thioredoxin YbbN regulates biofilm formation and cytotoxicity to enhance the pathogenicity of Vibrio parahaemolyticus, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

The thioredoxin family plays crucial roles in bacterial oxidative stress defenses and virulence regulation, while the function of its member YbbN in Vibrio parahaemolyticus remains unclear. [Objective] To elucidate the regulatory role of YbbN in the biological characteristics and pathogenicity of Vibrio parahaemolyticus, providing potential targets for developing novel anti-infection strategies. [Methods] The ybbN knockout strain (ΔybbN) and complementary strain (CΔybbN) of Vibrio parahaemolyticus SH112 were constructed by homologous recombination. The strains were compared regarding the growth characteristics, motility, biofilm formation, bacterial competition, cell adhesion, cytotoxicity, and pathogenicity in mice. [Results] Although the knockout of ybbN showed no significant effects on bacterial growth, motility, cell adhesion, or colonization, it markedly attenuated key pathogenic traits. Specifically, it decreased the biofilm formation (by 19%-30%), killing efficiency against competitive bacteria (*: P<0.05; ****: P<0.000 1), and cytotoxicity in HeLa cells (by 27%), while increasing the survival rate of mice by 87.5%. [Conclusion] This study demonstrates for the first time that YbbN specifically regulates critical aspects involved in biofilm formation, bacterial competition, and cytotoxicity in host cells, significantly influencing the biological characteristics and pathogenicity of Vibrio parahaemolyticus. These findings not only expand the understanding about the functional diversity of the thioredoxin family proteins but also provide new molecular targets and a theoretical basis for preventing Vibrio parahaemolyticus infections.

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E-mail: LI Tingting,
JIANG Wei,
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These authors contributed equally to this work.

, authorsList=Chuang RUI, Rong GUO, Shuqi LU, Peijie WU, Suoping QIU, Xiangan HAN, Wei JIANG, Tingting LI), CN=ArticleExt(id=1192150044833891139, articleId=1192149547934695511, tenantId=1146029695717560320, journalId=1192105938417971205, language=CN, title=硫氧还蛋白YbbN调控生物被膜形成及细胞毒性增强副溶血弧菌致病性, columnId=1192149544164012138, journalTitle=微生物学报, columnName=研究报告, runingTitle=null, highlight=null, articleAbstract=

硫氧还蛋白家族在细菌氧化应激防御和毒力调控中具有重要作用，但其成员YbbN蛋白在副溶血弧菌中的功能尚不明确。 【目的】 揭示YbbN蛋白对副溶血弧菌生物学特性和致病性的调控作用，为开发新型抗感染策略提供潜在靶点。 【方法】 使用同源重组技术构建副溶血弧菌SH112株的ybbN基因缺失株(ΔybbN)和互补株(CΔybbN)，比较各菌株的生长特性、运动性、生物被膜形成能力、细菌间竞争、细胞黏附、细胞毒性以及对小鼠的致病性。 【结果】 ybbN缺失不影响细菌生长、运动性、细胞黏附和定殖能力，削弱了副溶血弧菌的关键致病特性：生物被膜形成能力降低19%-30%，对大肠杆菌的杀伤效率极显著下降(*：P<0.05；****：P<0.000 1)，对HeLa细胞的毒性减弱27%，小鼠感染存活率提升87.5%。 【结论】 本研究阐明YbbN通过调控副溶血弧菌的生物被膜形成、细菌竞争和宿主细胞毒性等关键环节，显著影响其生物学特性和致病性。这一发现不仅拓展了对硫氧还蛋白家族蛋白功能多样性的认知，更为防控副溶血弧菌感染提供了新的分子靶标和理论依据。

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作者贡献声明

芮闯：实验操作、数据收集和撰写文章；郭容：实验操作、数据收集与监管、数据分析；卢淑淇：数据收集和监督管理；吴佩洁：软件程序和监督管理；邱索平：数据分析和监督管理；韩先干：研究构思和设计；蒋蔚：获取基金和项目管理；李婷婷：论文审阅和修改。

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A novel mouse model of enteric Vibrio parahaemolyticus infection reveals that the type III secretion system 2 effector VopC plays a key role in tissue invasion and gastroenteritis[J]. mBio, 2019, 10(6): e02608-19., articleTitle=A novel mouse model of enteric Vibrio parahaemolyticus infection reveals that the type III secretion system 2 effector VopC plays a key role in tissue invasion and gastroenteritis, refAbstract=null)], funds=[Fund(id=1192161173400338779, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, awardId=32473039, language=EN, fundingSource=the National Natural Science Foundation of China(32473039), fundOrder=null, country=null), Fund(id=1192161173480030556, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, awardId=32473039, language=CN, fundingSource=国家自然科学基金(32473039), fundOrder=null, country=null), Fund(id=1192161173547139421, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, awardId=21ZR1477000, language=EN, fundingSource=the Shanghai Natural Science Foundation(21ZR1477000), fundOrder=null, country=null), Fund(id=1192161173605859678, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, awardId=21ZR1477000, language=CN, fundingSource=上海市自然科学基金(21ZR1477000), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1192161167872246028, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, xref=1, ext=[AuthorCompanyExt(id=1192161167880634637, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161167872246028, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Shanghai University of Medicine & Health Sciences, Shanghai, China), AuthorCompanyExt(id=1192161167889023246, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161167872246028, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1上海健康医学院，上海)]), AuthorCompany(id=1192161167977103631, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, xref=2, ext=[AuthorCompanyExt(id=1192161167985492240, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161167977103631, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, China), AuthorCompanyExt(id=1192161167989686545, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161167977103631, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2中国农业科学院上海兽医研究所，上海)]), AuthorCompany(id=1192161168052601106, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, xref=3, ext=[AuthorCompanyExt(id=1192161168056795411, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161168052601106, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3Conghua Customs Comprehensive Technical Service Center, Guangzhou, Guangdong, China), AuthorCompanyExt(id=1192161168065184020, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, companyId=1192161168052601106, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3从化海关综合技术服务中心，广东 广州)])], figs=[ArticleFig(id=1192161171814891847, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 1, caption=PCR identification of ybbN gene deletion strain and its complementary strain. Lane M: DL2000 DNA marker; Lanes 1-7: Primers of WT-ybbN-E/F (2 538 bp), ΔybbN-ybbN-E/F (1 683 bp), CΔybbN-ybbN-E/F (1 683 bp), WT-ybbN-pMMB-F/R (873 bp), ΔybbN-ybbN-pMMB-F/R (no band), CΔybbN-ybbN-pMMB-F/R (873 bp), and ΔybbN-SacB-F/R (0 bp)., figureFileSmall=/qO52cAKaVUrC/F7npUfgA==, figureFileBig=q9xyufayw9Y22fmCwOsM/w==, tableContent=null), ArticleFig(id=1192161171928138056, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图1, caption=ybbN 基因缺失株及其互补株的PCR鉴定结果。M：DL2000 DNA marker；泳道1-7：WT-ybbN-E/F (2 538 bp)、ΔybbN-ybbN-E/F (1 683 bp)、CΔybbN-ybbN-E/F (1 683 bp)、WT-ybbN-pMMB-F/R (873 bp)、ΔybbN-ybbN-pMMB-F/R (无条带)、CΔybbN-ybbN-pMMB-F/R (873 bp)和ΔybbN-SacB-F/R (0 bp)片段。, figureFileSmall=/qO52cAKaVUrC/F7npUfgA==, figureFileBig=q9xyufayw9Y22fmCwOsM/w==, tableContent=null), ArticleFig(id=1192161172037189961, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 2, caption=Growth kinetics of Vibrio parahaemolyticus WT and mutant strains., figureFileSmall=zwAjZHR6KL57qlL/JlC9yg==, figureFileBig=/+RtE2XUvZEYjutBU1Xaxw==, tableContent=null), ArticleFig(id=1192161172100104522, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图2, caption=副溶血弧菌野生型与突变株生长动力学分析, figureFileSmall=zwAjZHR6KL57qlL/JlC9yg==, figureFileBig=/+RtE2XUvZEYjutBU1Xaxw==, tableContent=null), ArticleFig(id=1192161172163019083, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 3, caption=Motility analysis. A: Swimming motility of the strains; B: Swarming motility of the strains., figureFileSmall=+xPTqDg61pn62twaZ0+lng==, figureFileBig=1103eKMqv0sE3CEeVu/yQg==, tableContent=null), ArticleFig(id=1192161172242710860, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图3, caption=运动性分析。A：菌株的泳动运动；B：菌株的群集运动。, figureFileSmall=+xPTqDg61pn62twaZ0+lng==, figureFileBig=1103eKMqv0sE3CEeVu/yQg==, tableContent=null), ArticleFig(id=1192161172318208333, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 4, caption=Biofilm forming ability. A: Strains grown in LB at 30 ℃ and 37 ℃ for 48 h and stained with crystal violet; B: This shows the results of three independent experiments evaluating biofilm biomass (ns: P>0.05; *: P<0.05; ****: P<0.000 1)., figureFileSmall=7ODxoHFlO4zeNwbgMsGl1Q==, figureFileBig=SQMhT72NRsAp3a4M0HSIhg==, tableContent=null), ArticleFig(id=1192161172385317198, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图4, caption=生物被膜形成能力。A：菌株于30 ℃和37 ℃ LB中培养48 h后结晶紫染色；B：3次独立实验测定生物被膜生物量。, figureFileSmall=7ODxoHFlO4zeNwbgMsGl1Q==, figureFileBig=SQMhT72NRsAp3a4M0HSIhg==, tableContent=null), ArticleFig(id=1192161172477591887, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 5, caption=Antibacterial activity of Vibrio parahaemolyticus strains against Escherichia coli. Quantitative analysis of Escherichia coli (A) and Vibrio parahaemolyticus (B) pre- (0 h) and post- (4 h) co-culture at 30 ℃; Quantitative analysis of Escherichia coli (C) and Vibrio parahaemolyticus (D) pre- (0 h) and post- (4 h) co-culture at 37 ℃. ns: P>0.05; *: P<0.05; ****: P<0.000 1., figureFileSmall=dwyNvOvBAStGbuD+tnYBmg==, figureFileBig=WZDyLGuEIx3JbkXaRYCKpQ==, tableContent=null), ArticleFig(id=1192161172544700752, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图5, caption=各菌株对大肠杆菌的抗菌作用。30 ℃共培养前(0 h)及培养后(4 h)大肠杆菌(A)与副溶血弧菌(B)定量分析；37 ℃共培养前(0 h)及后(4 h)大肠杆菌(C)与副溶血弧菌(D)定量分析。, figureFileSmall=dwyNvOvBAStGbuD+tnYBmg==, figureFileBig=WZDyLGuEIx3JbkXaRYCKpQ==, tableContent=null), ArticleFig(id=1192161172590838097, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 6, caption=Adhesion to HeLa cell monolayers by various strains., figureFileSmall=lWl9jrq2kZ/Dd1bxUPdeww==, figureFileBig=TLibpm6+Pks86T+d07GmtA==, tableContent=null), ArticleFig(id=1192161172666335570, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图6, caption=各菌株对HeLa细胞的黏附作用, figureFileSmall=lWl9jrq2kZ/Dd1bxUPdeww==, figureFileBig=TLibpm6+Pks86T+d07GmtA==, tableContent=null), ArticleFig(id=1192161172737638739, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 7, caption=Cytotoxic effects of various strains on HeLa cells. ns: P>0.05; ****: P<0.000 1., figureFileSmall=g+fJ/1KDlnO+bgu5hfS/tA==, figureFileBig=DJx49VdtqVPetn29PLRIqA==, tableContent=null), ArticleFig(id=1192161172825719124, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图7, caption=各菌株对HeLa细胞的毒性作用, figureFileSmall=g+fJ/1KDlnO+bgu5hfS/tA==, figureFileBig=DJx49VdtqVPetn29PLRIqA==, tableContent=null), ArticleFig(id=1192161172901216597, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 8, caption=Survival rate of ICR mice infected with WT, ΔybbN, and CΔybbN strains., figureFileSmall=7f95huQxzSN+lxKhwUrrsQ==, figureFileBig=w7Bp6pzaBIq4bRANfiWRBw==, tableContent=null), ArticleFig(id=1192161172972519766, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图8, caption=WT、ΔybbN 和CΔybbN 攻毒后ICR小鼠存活率, figureFileSmall=7f95huQxzSN+lxKhwUrrsQ==, figureFileBig=w7Bp6pzaBIq4bRANfiWRBw==, tableContent=null), ArticleFig(id=1192161173056405847, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Figure 9, caption=Bacterial loads in mice infected with each strain. A: Heart; B: Liver; C: Spleen; D: Kidney., figureFileSmall=SNPlem3C0d+W61f4D66KgQ==, figureFileBig=MiAMYbgArs7EIYVYESH7TA==, tableContent=null), ArticleFig(id=1192161173127709016, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=图9, caption=各菌株在小鼠组织的细菌载量, figureFileSmall=SNPlem3C0d+W61f4D66KgQ==, figureFileBig=MiAMYbgArs7EIYVYESH7TA==, tableContent=null), ArticleFig(id=1192161173190623577, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=EN, label=Table 1, caption=

Primers used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
PrimersPrimer sequences (5′→3′)Restriction enzymeProduct size (bp)
ybbN-AACCGGATCCTCACGCACTAACCAGCAATABamH I588
ybbN-BCTGAGTGTCCTTGCTTTTAATTCAGGT
ybbN-CAGCAAGGACACTCAGGCGCAGAGTTCTTCTA409
ybbN-DACCGCATGCAAATGACCTCTTGTGCTGGAPst I
ybbN-EGTGCTCAAGGTGAAGGTCGC

Wide type: 2 538

Mutant: 1 683

ybbN-FTTGAGGATTTCTGCCTGACG
ybbN-pMMB-FATTCTGCAGATGCAATCCCCATTTATCGTPst I873
ybbN-pMMB-RACTGAGCTCTTAGTACAAGATGGAGTACASac I
SacB-FACGGCACTGTCGCAAACTATA600
SacB-RTTCCGTCACCGTCAAAGAT
), ArticleFig(id=1192161173274509658, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149547934695511, language=CN, label=表1, caption=

本研究所用引物

, figureFileSmall=null, figureFileBig=null, tableContent=
PrimersPrimer sequences (5′→3′)Restriction enzymeProduct size (bp)
ybbN-AACCGGATCCTCACGCACTAACCAGCAATABamH I588
ybbN-BCTGAGTGTCCTTGCTTTTAATTCAGGT
ybbN-CAGCAAGGACACTCAGGCGCAGAGTTCTTCTA409
ybbN-DACCGCATGCAAATGACCTCTTGTGCTGGAPst I
ybbN-EGTGCTCAAGGTGAAGGTCGC

Wide type: 2 538

Mutant: 1 683

ybbN-FTTGAGGATTTCTGCCTGACG
ybbN-pMMB-FATTCTGCAGATGCAATCCCCATTTATCGTPst I873
ybbN-pMMB-RACTGAGCTCTTAGTACAAGATGGAGTACASac I
SacB-FACGGCACTGTCGCAAACTATA600
SacB-RTTCCGTCACCGTCAAAGAT
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硫氧还蛋白YbbN调控生物被膜形成及细胞毒性增强副溶血弧菌致病性
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芮闯 1 , 郭容 2 , 卢淑淇 2 , 吴佩洁 3 , 邱索平 3 , 韩先干 2 , 蒋蔚 2 , 李婷婷 1
微生物学报 | 研究报告 2025,65(10): 4420-4430
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微生物学报 | 研究报告 2025, 65(10): 4420-4430
硫氧还蛋白YbbN调控生物被膜形成及细胞毒性增强副溶血弧菌致病性
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芮闯1, 郭容2, 卢淑淇2, 吴佩洁3, 邱索平3, 韩先干2, 蒋蔚2 , 李婷婷1
作者信息
  • 1上海健康医学院，上海
  • 2中国农业科学院上海兽医研究所，上海
  • 3从化海关综合技术服务中心，广东 广州
Thioredoxin YbbN regulates biofilm formation and cytotoxicity to enhance the pathogenicity of Vibrio parahaemolyticus
Chuang RUI1, Rong GUO2, Shuqi LU2, Peijie WU3, Suoping QIU3, Xiangan HAN2, Wei JIANG2 , Tingting LI1
Affiliations
  • 1Shanghai University of Medicine & Health Sciences, Shanghai, China
  • 2Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, China
  • 3Conghua Customs Comprehensive Technical Service Center, Guangzhou, Guangdong, China
出版时间: 2025-09-04 doi: 10.13343/j.cnki.wsxb.20250168
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摘要
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硫氧还蛋白家族在细菌氧化应激防御和毒力调控中具有重要作用，但其成员YbbN蛋白在副溶血弧菌中的功能尚不明确。 【目的】 揭示YbbN蛋白对副溶血弧菌生物学特性和致病性的调控作用，为开发新型抗感染策略提供潜在靶点。 【方法】 使用同源重组技术构建副溶血弧菌SH112株的ybbN基因缺失株(ΔybbN)和互补株(CΔybbN)，比较各菌株的生长特性、运动性、生物被膜形成能力、细菌间竞争、细胞黏附、细胞毒性以及对小鼠的致病性。 【结果】 ybbN缺失不影响细菌生长、运动性、细胞黏附和定殖能力，削弱了副溶血弧菌的关键致病特性：生物被膜形成能力降低19%-30%，对大肠杆菌的杀伤效率极显著下降(*：P<0.05；****：P<0.000 1)，对HeLa细胞的毒性减弱27%，小鼠感染存活率提升87.5%。 【结论】 本研究阐明YbbN通过调控副溶血弧菌的生物被膜形成、细菌竞争和宿主细胞毒性等关键环节，显著影响其生物学特性和致病性。这一发现不仅拓展了对硫氧还蛋白家族蛋白功能多样性的认知，更为防控副溶血弧菌感染提供了新的分子靶标和理论依据。

副溶血弧菌  /  硫氧还蛋白  /  YbbN  /  生物学特性  /  毒力调控

The thioredoxin family plays crucial roles in bacterial oxidative stress defenses and virulence regulation, while the function of its member YbbN in Vibrio parahaemolyticus remains unclear. [Objective] To elucidate the regulatory role of YbbN in the biological characteristics and pathogenicity of Vibrio parahaemolyticus, providing potential targets for developing novel anti-infection strategies. [Methods] The ybbN knockout strain (ΔybbN) and complementary strain (CΔybbN) of Vibrio parahaemolyticus SH112 were constructed by homologous recombination. The strains were compared regarding the growth characteristics, motility, biofilm formation, bacterial competition, cell adhesion, cytotoxicity, and pathogenicity in mice. [Results] Although the knockout of ybbN showed no significant effects on bacterial growth, motility, cell adhesion, or colonization, it markedly attenuated key pathogenic traits. Specifically, it decreased the biofilm formation (by 19%-30%), killing efficiency against competitive bacteria (*: P<0.05; ****: P<0.000 1), and cytotoxicity in HeLa cells (by 27%), while increasing the survival rate of mice by 87.5%. [Conclusion] This study demonstrates for the first time that YbbN specifically regulates critical aspects involved in biofilm formation, bacterial competition, and cytotoxicity in host cells, significantly influencing the biological characteristics and pathogenicity of Vibrio parahaemolyticus. These findings not only expand the understanding about the functional diversity of the thioredoxin family proteins but also provide new molecular targets and a theoretical basis for preventing Vibrio parahaemolyticus infections.

Vibrio parahaemolyticus  /  thioredoxin  /  YbbN  /  biological characteristics  /  virulence regulation
芮闯, 郭容, 卢淑淇, 吴佩洁, 邱索平, 韩先干, 蒋蔚, 李婷婷. 硫氧还蛋白YbbN调控生物被膜形成及细胞毒性增强副溶血弧菌致病性. 微生物学报, 2025 , 65 (10) : 4420 -4430 . DOI: 10.13343/j.cnki.wsxb.20250168
Chuang RUI, Rong GUO, Shuqi LU, Peijie WU, Suoping QIU, Xiangan HAN, Wei JIANG, Tingting LI. Thioredoxin YbbN regulates biofilm formation and cytotoxicity to enhance the pathogenicity of Vibrio parahaemolyticus[J]. Acta Microbiologica Sinica, 2025 , 65 (10) : 4420 -4430 . DOI: 10.13343/j.cnki.wsxb.20250168
正文
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副溶血弧菌(Vibrio parahaemolyticus)集中分布于温暖海域及河口环境，并在鱼类、虾类和贝类等水产品中广泛存在，是全球食源性疾病的主要病原体之一[1-2]。人类因摄食受副溶血弧菌污染的海鲜可引发急性胃肠炎[3]。在极少数情况下，该菌可经创面入侵引发致死性败血症[4]。作为全球性的关键食源致病菌，副溶血弧菌不仅严重制约水产养殖业发展，而且严重威胁公共卫生[5-6]。因此，解析副溶血弧菌致病性的潜在机制对于制定有效的控制措施和预防策略具有重要意义。
病原体具有一系列复杂的防御系统，其中硫氧还蛋白(thioredoxin, Trx)超家族的成员在调控氧化还原反应中发挥着重要作用[7]。Trx系统作为一种关键的抗氧化系统，通过其二硫键还原酶活性在防御氧化应激方面发挥核心作用，是细菌感染期间氧化还原调节的关键参与者，并在宿主-病原体相互作用中起到关键调控功能[8-9]。此外，Trx系统能够调控多种生理过程，如新陈代谢、运动性、宿主适应性、毒力表达和生物被膜的形成[10]。YbbN作为Trx家族的重要成员，其结构包含典型Trx结构域及可能的TPR结构域，虽缺乏传统Trx蛋白的氧化还原酶活性，但表现出独特的分子伴侣功能[11-12]。研究表明YbbN可通过直接结合底物或与GroEL互作发挥调控作用[13]。值得注意的是，Trx超家族成员功能多样，例如：大肠杆菌Trx家族蛋白DsbC在蛋白质折叠中发挥作用[14]；幽门螺杆菌中TrxA能够修复过氧化物损伤，促进胃黏膜定殖[15]。然而，目前在副溶血弧菌中关于Trx家族中YbbN对宿主致病性作用的机制仍知之甚少。
本研究通过同源重组技术构建了副溶血弧菌SH112株ybbN (vp0806)基因缺失株及其互补株，通过系统比较各菌株的生长特性、运动能力、生物被膜形成能力、细菌间竞争、细胞黏附、细胞毒性以及对小鼠的致病性，以期阐明Trx家族蛋白YbbN在副溶血弧菌生物学特性和致病性中的具体作用机制，为开发针对Trx系统的新型抗菌策略提供理论依据。
1 材料与方法
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1.1 菌种、质粒、试剂和实验动物
副溶血弧菌SH112株(tdh+，血清型O3:K6)、大肠杆菌HB101 (pRK2013)、CC118λpir、DH5α，质粒pYAK1和pMMB207，以及HeLa细胞均由本实验室保存；CytoTox 96®非放射性试剂盒购自Promega公司；分子克隆工具酶购自宝生物工程(大连)有限公司；DMEM细胞培养基和胎牛血清均购自Gibco公司；institute of cancer research (ICR)小鼠购自上海杰思捷实验动物有限公司。
1.2 引物设计与合成
本研究所用引物(表1)依据副溶血弧菌RIMD 2210633标准株的ybbN基因序列设计。以SacB-F/R为引物，通过PCR检测鉴定pYAK1在细菌中的凋亡情况。
1.3 ybbN基因缺失株与互补株的构建
参照文献[16]的方法构建基因缺失株。以野生株(wild type strain, WT)副溶血弧菌SH112株的基因组DNA为模板，采用引物对ybbN-A/B和ybbN-C/D分别扩增目标基因上、下游同源臂。随后，以ybbN-A/D为引物进行融合PCR，获得缺失片段ybbN-AD。将此片段双酶切后克隆至pYAK1载体，构建重组质粒pYAK1-ybbN，并转化大肠杆菌CC118λpir，获得重组菌株pYAK1-ybbN-CC118λpir。通过接合转移将重组菌株pYAK1-ybbN-CC118λpir导入WT，利用含10 μg/mL氯霉素的TCBS平板和含20%蔗糖的LB平板筛选接合子，并使用引物对ybbN-E/F和SacB-F/R进行PCR验证，缺失株命名为ΔybbN。
使用引物对ybbN-pMMB-F/R扩增ybbN基因完整ORF片段，连接至pMMB207载体，转化大肠杆菌CC118λpir感受态细胞，获得互补质粒pMMB-ybbN。通过接合转移将pMMB-ybbN导入ΔybbN，经引物ybbN-pMMB-F/R PCR鉴定阳性克隆，命名为互补株CΔybbN。
1.4 生长曲线测定
挑取WT、ΔybbN及CΔybbN单菌落，过夜培养后接种至含3% NaCl的LB液体培养基，37 ℃、180 r/min培养至对数生长期(OD600=0.20±0.02)。取100 μL菌液接种至96孔板，37 ℃静态孵育，每间隔1 h测定OD600，持续12 h，绘制生长曲线。
1.5 运动性测定
各取1 µL对数生长期菌液，垂直点样于泳动平板(含0.3%琼脂、3% NaCl的LB培养基)，37 ℃孵育4 h；同法加样于群集运动平板(含1.5%琼脂的BHI培养基)，30 ℃孵育16 h，测定迁移直径并记录表型。
1.6 生物被膜测定
取200 µL对数生长期菌液接种于96孔板，分别于30 ℃和37 ℃静置培养48 h，去除菌悬液，PBS洗涤后加入甲醇固定、结晶紫染色，PBS洗涤后自然风干。加入200 μL 95%乙醇溶解结晶紫，于酶标仪测定OD595。
1.7 细菌竞争试验
采用体外竞争模型评估WT、ΔybbN和CΔybbN对携带pBAD33-Gm质粒的大肠杆菌DH5α的杀伤能力。将各菌株培养至对数生长期，4×106副溶血弧菌和1×106大肠杆菌等体积混合。梯度稀释上述混合菌液后涂布TCBS培养基(筛选副溶血弧菌)及含庆大霉素(30 μg/mL)的LB平板(筛选大肠杆菌)，37 ℃培养过夜后计数，得培养前(0 h)的初始菌体浓度；另取100 µL菌液涂布LB平板，30 ℃/37 ℃培养4 h后回收菌体，计数得培养4 h的菌体浓度(CFU/mL)。
1.8 细胞黏附试验
HeLa细胞接种于含10% FBS-DMEM的24孔板，DMEM洗涤3次备用。取对数期WT、ΔybbN及CΔybbN菌液，空白DMEM洗涤后按MOI=100:1与细胞共孵育1 h。PBS洗涤3次，加入0.5% Triton X-100裂解细胞，裂解液用无菌PBS梯度稀释后涂布3% NaCl-LB平板，统计菌落数以评估相对黏附率。
1.9 细胞毒性检测
取对数期菌悬液，以MOI=100:1感染HeLa细胞，37 ℃孵育1.5 h (设同步对照组)。按CytoTox96®试剂盒说明书检测细胞上清乳酸脱氢酶释放水平，量化细胞毒性。
1.10 小鼠存活试验
参照白雪瑞等[17]方法，将3-4周龄ICR雌鼠分为WT组、ΔybbN组、CΔybbN组和空白组，每组8只，腹腔注射100 μL对数期菌悬液(3×108 CFU/mL)或生理盐水。每隔1 h观察1次，连续记录7 d存活率。
本研究动物实验获中国农业科学院上海兽医研究所实验动物福利与伦理管理委员会批准，编号为SV-20211231-G04。
1.11 组织载量测定
五周龄ICR小鼠随机分为4组(WT、ΔybbN、CΔybbN及空白对照，n=10)，腹腔注射100 μL对数期菌液(5×107 CFU/mL)或生理盐水。感染10 h后随机处死各组5只小鼠，无菌解剖观察脏器病理变化。取心、肝、脾、肾组织制备匀浆，PBS梯度稀释后涂布TCBS平板，计算各脏器载菌量。
1.12 数据分析
定量数据采用GraphPad Prism 8软件进行单因素方差分析(one-way ANOVA)，结果以mean±SD表示，显著性阈值为P<0.05。
2 结果与分析
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2.1 缺失株ΔybbN和互补株CΔybbN的鉴定
经ybbN-E/F引物PCR扩增，WT呈现2 538 bp特征条带(图1，泳道1)，而ΔybbN和CΔybbN均获得1 683 bp条带(图1，泳道2、3)，测序比对证实成功缺失855 bp的ybbN基因片段。采用ybbN-pMMB-F/R引物扩增时，WT和互补株CΔybbN均呈现873 bp互补载体特征条带(图1，泳道4、6)，ΔybbN则无扩增条带(图1，泳道5)。经20代传代培养后，SacB-F/R引物在ΔybbN中无扩增(图1，泳道7)，证实自杀载体pYAK1已成功消除。上述结果表明ybbN基因缺失株ΔybbN和互补株CΔybbN构建成功。
2.2 ybbN基因不影响副溶血弧菌的生长特性
如图2所示，ΔybbN与WT、CΔybbN的生长速率无显著差异(P>0.05)，表明ybbN缺失未显著改变副溶血弧菌的生长特性。
2.3 YbbN不参与副溶血弧菌运动
泳动平板培养4 h后各菌株均形成典型半透明迁移环(图3A)，ΔybbN的泳动能力与WT和CΔybbN相比差异无统计学意义(P>0.05，图3B)。所有菌株均表现出明显的群集运动能力(图3C)，ΔybbN的群集运动能力与WT相比差异也不显著(P>0.05，图3D)。结果表明ybbN缺失不影响细菌运动性。
2.4 生物被膜形成分析
如图4所示，ΔybbN在30 ℃的生物被膜形成能力较WT下降19% (*：P<0.05)，在37 ℃下降30% (***：P<0.001)，且温度升高加剧表型缺失，而CΔybbN与WT差异无统计学意义(P>0.05)。提示YbbN在温暖环境中对生物被膜形成具有关键调控作用。
2.5 YbbN介导副溶血弧菌细菌竞争
细菌竞争试验结果(图5A、5C)显示，在30 ℃和37 ℃条件下，ΔybbN组大肠杆菌存活率较WT显著升高(*：P<0.05；****：P<0.000 1)。互补株CΔybbN在30 ℃和37 ℃均恢复抗菌活性。副溶血弧菌活菌计数结果(图5B、5D)表明，各组细菌在共培养期间生长速率差异无统计学意义(P>0.05)，排除了生长缺陷所致抗菌活性变化的可能。结果提示ybbN参与了副溶血弧菌对大肠杆菌的抗菌作用。
2.6 ybbN不参与副溶血弧菌细胞黏附作用
细胞黏附实验结果(图6)显示，ΔybbN与WT的宿主细胞黏附效率差异无统计学意义(P>0.05)，表明ybbN缺失未显著改变副溶血弧菌的黏附能力。
2.7 ybbN缺失降低副溶血弧菌细胞毒性
细胞毒性结果显示(图7)表明，ΔybbN的细胞毒性较WT显著降低27% (****：P<0.000 1)，证实ybbN是副溶血弧菌毒力的关键调控因子。
2.8 ybbN缺失对副溶血弧菌毒力的影响
如图8所示，WT组小鼠于感染2 h出现急性呼吸窘迫伴水样腹泻，并迅速全部死亡；ΔybbN组临床表现明显减轻，死亡延迟，存活率达87.5%；CΔybbN组重现WT组的表型，存活率为12.5%。对照组无异常，存活率为100.0%。结果表明ybbN缺失显著降低副溶血弧菌毒力，提示该基因参与致病过程。
2.9 ybbN缺失不影响副溶血弧菌小鼠组织定殖
如图9所示，与WT相比，ΔybbN在小鼠心脏、肝脏、脾脏和肾脏的细菌载量差异无统计学意义(P>0.05)，表明ybbN不参与副溶血弧菌在小鼠组织的定殖。
3 讨论与结论
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Trx家族蛋白在微生物中广泛存在，不仅在脱氧核糖核苷酸合成等基础代谢中发挥核心作用，还作为多种还原酶的关键底物参与细胞氧化还原调控[18]。Trx系统不仅调控细菌运动性、宿主适应、毒力表达和生物被膜形成等功能，还帮助细菌适应环境变化[19-21]。例如，鲍曼不动杆菌trxA突变体已被提出作为潜在减毒活疫苗[22]。目前，关于Trx家族成员YbbN在副溶血弧菌环境适应及致病机制中的研究仍明显不足。生物信息学分析显示，副溶血弧菌YbbN具有独特结构，包含Trx结构域及TPR_19和TPR_20两个结构域。本研究构建了ybbN缺失株和互补株，系统解析了YbbN在副溶血弧菌致病过程中的分子机制。
生物被膜是细菌抵御环境胁迫的关键屏障，其形成与毒力密切相关并受多因素精细调控[23]。研究表明Trx是鲍曼不动杆菌和杀鱼爱德华氏菌等多种病原菌生物被膜形成的关键因子[24-25]。本研究发现，ybbN缺失不影响副溶血弧菌生长和运动，但在30 ℃和37 ℃均显著削弱其生物被膜形成；细菌竞争试验也显示ΔybbN对大肠杆菌的杀伤能力明显下降。Trx通过向二硫键系统提供电子并帮助错误配对二硫键异构化，促使蛋白正确折叠，在毒力调控中起核心作用[26]。YbbN可能借助Trx系统影响抗菌物质及生物被膜相关蛋白的折叠，从而增强副溶血弧菌的环境生存能力。本研究结果证实YbbN调控副溶血弧菌生物被膜形成与种间竞争，提示其可能是副溶血弧菌适应环境的关键因子。
副溶血弧菌通过毒力因子破坏宿主细胞结构，驱动体内增殖并介导疾病[5,27]。研究显示，Trx可促进特定毒力因子表达、诱导抗氧化应激并触发过度免疫应答，进而调控细菌毒力[8,24]。链球菌中TrxA通过维持T3SS效应蛋白折叠直接增强毒力[10]。本研究揭示YbbN具有独特致病调控模式：虽然不参与HeLa细胞黏附及小鼠组织定殖，但ybbN缺失使细胞毒性降低27%，小鼠存活率提高至87.5%，提示其可能通过底物选择性伴侣机制影响特定毒力因子折叠，进而促进副溶血弧菌毒力。该发现为理解Trx家族蛋白在细菌致病中的多样化功能提供了新视角。
本研究系统阐明了YbbN在副溶血弧菌环境适应和致病过程中的作用。ybbN缺失在不影响生长、运动、黏附及定殖的同时，显著削弱生物被膜形成、抗菌活性、细胞毒力和小鼠致病性。我们推测YbbN通过以下机制调控毒力：(1) 维持氧化还原稳态，确保毒力因子正确折叠；(2) 调控抗菌物质分泌，增强环境竞争优势；(3) 促进生物被膜形成，提高环境适应性。鉴于YbbN在毒力调控中的独特作用且对基本生理无明显影响，该蛋白可作为副溶血弧菌减毒疫苗的理想靶标。本研究拓展了Trx家族蛋白功能多样性的认识，为深入解析副溶血弧菌致病机制提供了新的理论框架和研究方向。
基金
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  • 国家自然科学基金(32473039)
  • 上海市自然科学基金(21ZR1477000)
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2025年第65卷第10期
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文章信息
doi: 10.13343/j.cnki.wsxb.20250168
  • 接收时间：2025-03-03
  • 首发时间：2025-11-03
  • 出版时间：2025-09-04
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  • 收稿日期：2025-03-03
  • 录用日期：2025-05-12
基金
the National Natural Science Foundation of China(32473039)
国家自然科学基金(32473039)
the Shanghai Natural Science Foundation(21ZR1477000)
上海市自然科学基金(21ZR1477000)
作者信息
    1上海健康医学院，上海
    2中国农业科学院上海兽医研究所，上海
    3从化海关综合技术服务中心，广东 广州
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https://castjournals.cast.org.cn/joweb/wswxb/CN/10.13343/j.cnki.wsxb.20250168
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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