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Article(id=1226460580471550923, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250119, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1739894400000, receivedDateStr=2025-02-19, revisedDate=null, revisedDateStr=null, acceptedDate=1742313600000, acceptedDateStr=2025-03-19, onlineDate=1770340588920, onlineDateStr=2026-02-06, pubDate=1754236800000, pubDateStr=2025-08-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770340588920, onlineIssueDateStr=2026-02-06, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770340588920, creator=13701087609, updateTime=1770340588920, updator=13701087609, issue=Issue{id=1226460576751206672, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='8', pageStart='1', pageEnd='3812', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770340588033, creator=13701087609, updateTime=1770363610188, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1226557138735117113, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1226557138735117114, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1226460576751206672, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3782, endPage=3793, ext={EN=ArticleExt(id=1226460581306217465, articleId=1226460580471550923, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=A multiplex PCR method for identification of virulent strains of Streptococcus suis serotype 4, columnId=1194702985843413943, journalTitle=Acta Microbiologica Sinica, columnName=Technology and Method, runingTitle=null, highlight=null, articleAbstract=

Streptococcus suis is a major pathogen in pigs and also a zoonotic pathogen. This bacterium has numerous serotypes, among which S. suis serotype 4 (SS4) is known to infect humans and poses a threat to public health due to its potential high pathogenicity. [Objective] To develop a multiplex PCR method based on specific virulence-associated genes of SS4 virulent strains to achieve precise identification of such strains. [Methods] Based on previous research results, four target genes specific to SS4 virulent strains—sly, igdE, tran, and sao—were selected, and the SS4 serotype-specific gene wzy was used as an internal reference gene to design a pentaplex PCR method. After optimization of the multiplex PCR amplification system, specificity and sensitivity tests were conducted. This method was then employed to detect newly isolated SS4 strains. Additionally, zebrafish virulence assays were performed to validate the accuracy of this method. [Results] The multiplex PCR method specifically amplified the target genes, effectively distinguishing SS4 virulent strains from lowly virulent strains. The method exhibited high sensitivity, with a minimum detection limit of 4.1×102 CFU or 12.5 pg of genomic DNA. Specificity validation confirmed that this method accurately identified SS4 virulent strains. This method was then employed to examine six clinically isolated SS4 strains. Three strains were identified as virulent, showing high pathogenicity in zebrafish and causing a mortality rate of 60.00%-86.67%. The other three strains were identified as lowly virulent strains, exhibiting low pathogenicity in zebrafish and causing a mortality rate of 0-6.67%. [Conclusion] A multiplex PCR method based on virulence-associated genes of S. suis was successfully developed, enabling accurate and sensitive identification of SS4 virulent strains. This method provides technical support for the early diagnosis and effective prevention and control of S. suis infections.

, correspAuthors=Zongfu WU, authorNote=null, correspAuthorsNote=
*E-mail:
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猪链球菌(Streptococcus suis)不仅是猪的重要致病菌，还是一种人兽共患病原体。该菌血清型众多，其中血清4型(SS4)属于可感染人类的血清型，因其潜在的高致病性，对公共卫生构成威胁。 【目的】 开发一种基于SS4毒力株特有毒力相关基因的多重PCR方法，以实现SS4毒力株的精准鉴定。 【方法】 基于前期研究，选择sly、igdE、tran和sao这4个SS4毒力株特有的靶基因，结合SS4血清型特异基因wzy作为内参基因，设计了一套五重PCR方法。通过优化多重PCR扩增体系，进行了特异性和敏感性试验，并应用该方法检测新分离的SS4菌株。同时，结合斑马鱼毒力试验验证该方法的准确性。 【结果】 该多重PCR方法能特异性扩增靶基因，有效区分SS4毒力株与弱毒株。其敏感性高，最低可检测到4.1×102 CFU的菌落数或12.5 pg的基因组DNA。特异性验证表明，该方法能准确辨识SS4毒力株。利用该方法检测临床分离的6株SS4菌株：3株菌株被鉴定为毒力株，对斑马鱼的致病性较高，死亡率为60.00%-86.67%；3株被鉴定为弱毒株的菌株对斑马鱼的致病性低，死亡率为0-6.67%。 【结论】 本研究开发了一种基于猪链球菌毒力相关基因的多重PCR方法，能够准确、灵敏地鉴定SS4毒力株，为猪链球菌病的早期诊断和有效防控提供了技术支撑。

, correspAuthors=吴宗福, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=j+mXhzY2NpqFCGFcj37+MA==, magXml=1zXW8Ir1U+3y/bGy6Y0EUQ==, pdfUrl=null, pdf=hs6YL2egUsGcyKOEl33NPQ==, pdfFileSize=1714843, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=TtfZKatd9yUon/4b41Lojg==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=4ZWq806ZpN7OJjnmFhtDhA==, mapNumber=null, authorCompany=null, fund=null, authors=

作者贡献声明

朱金鲁：方法论，数据分析，完成呈现，撰写文章，编辑、审阅；彭泽仁：软件程序；庄鸿琨：验证；孙洁：提供资源；吴宗福：提出概念，方法论，编辑、撰写、审阅，项目管理，获取基金。

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Provincial Key Laboratory of Research on the Technology of Pig-breeding and Pig-disease Prevention, Guangdong Haid Institute of Animal Husbandry & Veterinary, Guangzhou, Guangdong, China), AuthorCompanyExt(id=1226596293393432734, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, companyId=1226596293376655515, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=5.广东省养猪与猪病防控技术研究企业重点实验室，广东海大畜牧兽医研究院，广东 广州)])], figs=[ArticleFig(id=1226596297956835815, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Figure 1, caption=Distribution of virulence-associated genes in virulent and lowly virulent strains of Streptococcus suis serotype 4., figureFileSmall=Lnz8MobuyLuULFBYdxWDqg==, figureFileBig=sMK72IBnUmMZcLVsq/pKig==, tableContent=null), ArticleFig(id=1226596298107830772, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=图1, caption=猪链球菌4型毒力株与弱毒株毒力相关基因分布, figureFileSmall=Lnz8MobuyLuULFBYdxWDqg==, figureFileBig=sMK72IBnUmMZcLVsq/pKig==, tableContent=null), ArticleFig(id=1226596298246242813, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Figure 2, caption=The results of single plex PCR and multiplex (5-plex) PCR amplification. A: Single plex PCR (lanes 1-5) and multiplex PCR (5-plex, lane 6) amplification using the virulent strain 2021WUSS075 of S. suis serotype 4 as the template; B: Single plex PCR (lanes 1-5) and multiplex PCR (5-plex, lane 6) amplification using the lowly virulent strain 2022WUSS056 of S. suis serotype 4 as the template. M: DL2000 DNA marker; N: Blank control (H2O as template); -: The absence of specific target bands; +: The presence of specific target bands., figureFileSmall=S7Bxvt0u6xvHrHbt46DaqQ==, figureFileBig=0r5OMpPBqkXH6NPXWXPalA==, tableContent=null), ArticleFig(id=1226596298355294724, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=图2, caption=单重PCR和五重PCR扩增。A：猪链球菌4型毒力株2021WUSS075为模板进行单重PCR (泳道1-5)和五重PCR (泳道6)扩增；B：以猪链球菌4型弱毒株2022WUSS056为模板进行单重PCR (泳道1-5)和五重PCR (泳道6)扩增。M：DL2000 DNA marker；N：空白对照(以H2O为模板)；-代表无特异性目的条带；+代表有特异性目的条带。, figureFileSmall=S7Bxvt0u6xvHrHbt46DaqQ==, figureFileBig=0r5OMpPBqkXH6NPXWXPalA==, tableContent=null), ArticleFig(id=1226596299718443531, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Figure 3, caption=Sensitivity and specificity of multiplex PCR. A: Using the bacterial culture of virulent strain 2021WUSS075 as the template (Lanes 1-6: 4.1×105, 4.1×104, 4.1×103, 4.1×102, 4.1×101, and 4.1×100 CFU); B: Using the genomic DNA of virulent strain 2021WUSS075 as the template (Lanes 1-6: 12.5 ng, 1.25 ng, 0.125 ng, 12.5 pg, 1.25 pg, and 0.125 pg); C: Specificity of multiplex PCR for different S. suis serotypes (Lanes 1-11: serotype 4 (2021WUSS075), serotype 1/2 (2023WUSS108), serotype 1 (2023WUSS142), serotype 2 (ZJWUSS065), serotype 3 (SZWUSS009), serotype 5 (SZWUSS051), serotype 6 (2023WUSS088), serotype 7 (2023WUSS049), serotype 8 (SZWUSS056), serotype 9 (SZWUSS029), and serotype 14 (2022WUSS024)); D: Specificity of multiplex PCR against non-S. suis strains (Lanes 1-9: Positive control (S. suis serotype 4 strain 2021WUSS075), E. coli, G. parasuis, A. pleuropneumoniae, S. aureus, Enterococcus spp., S. pasteurianus, S. equi subsp. zooepidemicus, and S. agalactiae; N: Blank control (H2O as template))., figureFileSmall=MIJXtX7E+XDBRqRXPPnikQ==, figureFileBig=SEfup5+jL7c1l3MG18xb2A==, tableContent=null), ArticleFig(id=1226596299877827091, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=图3, caption=多重PCR的敏感性与特异性。A：以毒力株2021WUSS075细菌培养液为模板(泳道1-6：4.1×105、4.1×104、4.1×103、4.1×102、4.1×101、4.1×100 CFU)；B：以毒力株2021WUSS075基因组DNA为模板(泳道1-6：12.5 ng、1.25 ng、0.125 ng、12.5 pg、1.25 pg、0.125 pg)；C：针对猪链球菌不同血清型的多重PCR特异性验证(泳道1-11：血清4型2021WUSS075、1/2型2023WUSS108、1型2023WUSS142、2型ZJWUSS065、3型SZWUSS009、5型SZWUSS051、6型2023WUSS088、7型2023WUSS049、8型SZWUSS056、9型SZWUSS029、14型2022WUSS024)；D：针对非猪链球菌的多重PCR特异性验证[泳道1-9：阳性对照(猪链球菌4型菌株2021WUSS075)、大肠杆菌、副猪格拉菌、胸膜肺炎放线杆菌、金黄色葡萄球菌、肠球菌属、巴氏链球菌、马链球菌兽疫亚种以及无乳链球菌；N：空白对照(以H2O为模板)]。, figureFileSmall=MIJXtX7E+XDBRqRXPPnikQ==, figureFileBig=SEfup5+jL7c1l3MG18xb2A==, tableContent=null), ArticleFig(id=1226596300033016352, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Figure 4, caption=The results of multiplex PCR for newly isolated strains of Streptococcus suis serotype 4. V indicates a virulent strain control; L indicates a lowly virulent strain control; Lanes 1-6: Newly isolated strains of S. suis serotype 4, namely ZJWUSS044, SZWUSS010, SZWUSS047, SZWUSS048, SZWUSS0137, and SZWUSS0138; N: Blank control (H2O as template)., figureFileSmall=EaVF7Elex5bQ+tJvBUa+/w==, figureFileBig=BzeSaBUHNubanLGK620b0A==, tableContent=null), ArticleFig(id=1226596300188205615, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=图4, caption=猪链球菌4型新分离株的多重PCR鉴定。V代表毒力株对照；L代表弱毒株对照；泳道1-6：猪链球菌4型新分离菌株ZJWUSS044、SZWUSS010、SZWUSS047、SZWUSS048、SZWUSS0137、SZWUSS0138；N：空白对照(以H2O为模板)。, figureFileSmall=EaVF7Elex5bQ+tJvBUa+/w==, figureFileBig=BzeSaBUHNubanLGK620b0A==, tableContent=null), ArticleFig(id=1226596300305646137, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Table 1, caption=

The information of Streptococcus suis strains used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsSerotypeDateHostIsolation sourceVirulence level
ND9042014Diseased pigLungV
WUSS40642017Healthy pigTonsilV
2018WUSS01142018Healthy pigTonsilV
2021WUSS07542021Healthy pigTonsilV
2018WUSS15642018Diseased pig/V
ID3605442011Homo sapiensBloodV
WUSS34642017Healthy pigTonsilV
2018WUSS16042018Diseased pigSpleenV
WUSS30942017Healthy pigTonsilL
WUSS39942017Healthy pigTonsilL
2018WUSS05642018Healthy pigTonsilL
2020WUSS05942020Healthy pigTonsilL
2022WUSS01842022Healthy pigTonsilL
2022WUSS01942022Healthy pigTonsilL
2022WUSS05642022Healthy pigTonsilL
2022WUSS14142022Healthy pigTonsilL
2023WUSS1081/22023Healthy pigTonsil/
2023WUSS14212023Healthy pigTonsil/
ZJWUSS06522024Diseased pigBrain/
SZWUSS00932024Healthy pigTonsil/
SZWUSS05152024Healthy pigTonsil/
2023WUSS08862023Healthy pigTonsil/
2023WUSS04972023Healthy pigTonsil/
SZWUSS05682024Healthy pigTonsil/
SZWUSS02992024Healthy pigTonsil/
2022WUSS024142022Healthy pigTonsil/
ZJWUSS04442024Diseased pigLung/
SZWUSS01042024Healthy pigTonsil/
SZWUSS04742024Healthy pigTonsil/
SZWUSS04842024Healthy pigTonsil/
SZWUSS013742024Healthy pigTonsil/
SZWUSS013842024Healthy pigTonsil/
), ArticleFig(id=1226596300427280964, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=表1, caption=

本研究所用 Streptococcus suis 菌株信息

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsSerotypeDateHostIsolation sourceVirulence level
ND9042014Diseased pigLungV
WUSS40642017Healthy pigTonsilV
2018WUSS01142018Healthy pigTonsilV
2021WUSS07542021Healthy pigTonsilV
2018WUSS15642018Diseased pig/V
ID3605442011Homo sapiensBloodV
WUSS34642017Healthy pigTonsilV
2018WUSS16042018Diseased pigSpleenV
WUSS30942017Healthy pigTonsilL
WUSS39942017Healthy pigTonsilL
2018WUSS05642018Healthy pigTonsilL
2020WUSS05942020Healthy pigTonsilL
2022WUSS01842022Healthy pigTonsilL
2022WUSS01942022Healthy pigTonsilL
2022WUSS05642022Healthy pigTonsilL
2022WUSS14142022Healthy pigTonsilL
2023WUSS1081/22023Healthy pigTonsil/
2023WUSS14212023Healthy pigTonsil/
ZJWUSS06522024Diseased pigBrain/
SZWUSS00932024Healthy pigTonsil/
SZWUSS05152024Healthy pigTonsil/
2023WUSS08862023Healthy pigTonsil/
2023WUSS04972023Healthy pigTonsil/
SZWUSS05682024Healthy pigTonsil/
SZWUSS02992024Healthy pigTonsil/
2022WUSS024142022Healthy pigTonsil/
ZJWUSS04442024Diseased pigLung/
SZWUSS01042024Healthy pigTonsil/
SZWUSS04742024Healthy pigTonsil/
SZWUSS04842024Healthy pigTonsil/
SZWUSS013742024Healthy pigTonsil/
SZWUSS013842024Healthy pigTonsil/
), ArticleFig(id=1226596300532138568, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Table 2, caption=

Primer used in the study

, figureFileSmall=null, figureFileBig=null, tableContent=
Target genesAnnotation/FunctionPrimers namePrimer sequences (5′→3′)Size (bp)
slySuilysinsly-FACTTACGAGCCACAAGAGATT1 048
sly-RCACTGCTATTATGGACTGTTGA
igdECysteine protease IgdEigdE-FGCTTCCTGCTTATGTTGTTGTTG840
igdE-RGCTGAGATTGTTTCCTGTGTTGA
wzyWzy polymerasewzy-FGACTGGTTATTTGACAGCGATT604
wzy-RAACAGTGGCAAGCAATACAAAG
tranTranscriptional regulatortran-FGGTTCAAGACTGGAAGAATTACGA453
tran-RGAGGAGATTGGCATTATCAACTGA
saoSurface antigen onesao-FATGGTGGACTTGGCGATATT208
sao-RGTCATTGCTTCCTTAGAGACTT
), ArticleFig(id=1226596300683133522, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=表2, caption=

本研究所用引物

, figureFileSmall=null, figureFileBig=null, tableContent=
Target genesAnnotation/FunctionPrimers namePrimer sequences (5′→3′)Size (bp)
slySuilysinsly-FACTTACGAGCCACAAGAGATT1 048
sly-RCACTGCTATTATGGACTGTTGA
igdECysteine protease IgdEigdE-FGCTTCCTGCTTATGTTGTTGTTG840
igdE-RGCTGAGATTGTTTCCTGTGTTGA
wzyWzy polymerasewzy-FGACTGGTTATTTGACAGCGATT604
wzy-RAACAGTGGCAAGCAATACAAAG
tranTranscriptional regulatortran-FGGTTCAAGACTGGAAGAATTACGA453
tran-RGAGGAGATTGGCATTATCAACTGA
saoSurface antigen onesao-FATGGTGGACTTGGCGATATT208
sao-RGTCATTGCTTCCTTAGAGACTT
), ArticleFig(id=1226596300817351257, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=EN, label=Table 3, caption=

The results of the zebrafish infection experiment

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsDeaths in each period

Total

deaths

Mortality rate (%)P valueSignificance
12 h24 h36 h48 h60 h72 h84 h96 h
ZJWUSS044146020001386.670.000 6***
SZWUSS0100000000000.00<0.000 1****
SZWUSS047246010001386.670.003 2**
SZWUSS04824210000960.000.001 5**
SZWUSS01370000000000.00<0.000 1****
SZWUSS01380001000016.67<0.000 1****
SC0707315910000015100.00--
SH0409170000000000.00<0.000 1****
PBS0000000000.00<0.000 1****
), ArticleFig(id=1226596300951568990, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1226460580471550923, language=CN, label=表3, caption=

斑马鱼毒力试验

, figureFileSmall=null, figureFileBig=null, tableContent=
StrainsDeaths in each period

Total

deaths

Mortality rate (%)P valueSignificance
12 h24 h36 h48 h60 h72 h84 h96 h
ZJWUSS044146020001386.670.000 6***
SZWUSS0100000000000.00<0.000 1****
SZWUSS047246010001386.670.003 2**
SZWUSS04824210000960.000.001 5**
SZWUSS01370000000000.00<0.000 1****
SZWUSS01380001000016.67<0.000 1****
SC0707315910000015100.00--
SH0409170000000000.00<0.000 1****
PBS0000000000.00<0.000 1****
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猪链球菌血清4型毒力株鉴定多重PCR方法的建立
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朱金鲁 1, 2, 3 , 彭泽仁 1, 2, 3 , 庄鸿琨 1, 2, 3 , 孙洁 4 , 吴宗福 1, 2, 3, 5, *
微生物学报 | 技术与方法 2025,65(8): 3782-3793
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微生物学报 | 技术与方法 2025, 65(8): 3782-3793
猪链球菌血清4型毒力株鉴定多重PCR方法的建立
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朱金鲁1, 2, 3, 彭泽仁1, 2, 3, 庄鸿琨1, 2, 3, 孙洁4, 吴宗福1, 2, 3, 5, *
作者信息
  • 1.南京农业大学 动物医学院，江苏 南京
  • 2.农业部动物细菌学重点实验室，江苏 南京
  • 3.世界动物卫生组织猪链球菌病参考实验室，江苏 南京
  • 4.深圳海关动植物检验检疫技术中心，广东 深圳
  • 5.广东省养猪与猪病防控技术研究企业重点实验室，广东海大畜牧兽医研究院，广东 广州
A multiplex PCR method for identification of virulent strains of Streptococcus suis serotype 4
Jinlu ZHU1, 2, 3, Zeren PENG1, 2, 3, Hongkun ZHUANG1, 2, 3, Jie SUN4, Zongfu WU1, 2, 3, 5, *
Affiliations
  • 1.College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu, China
  • 2.Key Lab of Animal Bacteriology, Ministry of Agriculture and Rural Affairs, Nanjing, Jiangsu, China
  • 3.WOAH Reference Lab for Swine Streptococcosis, Nanjing, Jiangsu, China
  • 4.Animal and Plant Inspection and Quarantine Technology Centre of Shenzhen Customs, Shenzhen, Guangdong, China
  • 5.Guangdong Provincial Key Laboratory of Research on the Technology of Pig-breeding and Pig-disease Prevention, Guangdong Haid Institute of Animal Husbandry & Veterinary, Guangzhou, Guangdong, China
出版时间: 2025-08-04 doi: 10.13343/j.cnki.wsxb.20250119
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摘要
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猪链球菌(Streptococcus suis)不仅是猪的重要致病菌，还是一种人兽共患病原体。该菌血清型众多，其中血清4型(SS4)属于可感染人类的血清型，因其潜在的高致病性，对公共卫生构成威胁。 【目的】 开发一种基于SS4毒力株特有毒力相关基因的多重PCR方法，以实现SS4毒力株的精准鉴定。 【方法】 基于前期研究，选择sly、igdE、tran和sao这4个SS4毒力株特有的靶基因，结合SS4血清型特异基因wzy作为内参基因，设计了一套五重PCR方法。通过优化多重PCR扩增体系，进行了特异性和敏感性试验，并应用该方法检测新分离的SS4菌株。同时，结合斑马鱼毒力试验验证该方法的准确性。 【结果】 该多重PCR方法能特异性扩增靶基因，有效区分SS4毒力株与弱毒株。其敏感性高，最低可检测到4.1×102 CFU的菌落数或12.5 pg的基因组DNA。特异性验证表明，该方法能准确辨识SS4毒力株。利用该方法检测临床分离的6株SS4菌株：3株菌株被鉴定为毒力株，对斑马鱼的致病性较高，死亡率为60.00%-86.67%；3株被鉴定为弱毒株的菌株对斑马鱼的致病性低，死亡率为0-6.67%。 【结论】 本研究开发了一种基于猪链球菌毒力相关基因的多重PCR方法，能够准确、灵敏地鉴定SS4毒力株，为猪链球菌病的早期诊断和有效防控提供了技术支撑。

猪链球菌  /  血清4型  /  毒力株  /  多重PCR

Streptococcus suis is a major pathogen in pigs and also a zoonotic pathogen. This bacterium has numerous serotypes, among which S. suis serotype 4 (SS4) is known to infect humans and poses a threat to public health due to its potential high pathogenicity. [Objective] To develop a multiplex PCR method based on specific virulence-associated genes of SS4 virulent strains to achieve precise identification of such strains. [Methods] Based on previous research results, four target genes specific to SS4 virulent strains—sly, igdE, tran, and sao—were selected, and the SS4 serotype-specific gene wzy was used as an internal reference gene to design a pentaplex PCR method. After optimization of the multiplex PCR amplification system, specificity and sensitivity tests were conducted. This method was then employed to detect newly isolated SS4 strains. Additionally, zebrafish virulence assays were performed to validate the accuracy of this method. [Results] The multiplex PCR method specifically amplified the target genes, effectively distinguishing SS4 virulent strains from lowly virulent strains. The method exhibited high sensitivity, with a minimum detection limit of 4.1×102 CFU or 12.5 pg of genomic DNA. Specificity validation confirmed that this method accurately identified SS4 virulent strains. This method was then employed to examine six clinically isolated SS4 strains. Three strains were identified as virulent, showing high pathogenicity in zebrafish and causing a mortality rate of 60.00%-86.67%. The other three strains were identified as lowly virulent strains, exhibiting low pathogenicity in zebrafish and causing a mortality rate of 0-6.67%. [Conclusion] A multiplex PCR method based on virulence-associated genes of S. suis was successfully developed, enabling accurate and sensitive identification of SS4 virulent strains. This method provides technical support for the early diagnosis and effective prevention and control of S. suis infections.

Streptococcus suis  /  serotype 4  /  virulent strains  /  multiplex PCR
朱金鲁, 彭泽仁, 庄鸿琨, 孙洁, 吴宗福. 猪链球菌血清4型毒力株鉴定多重PCR方法的建立. 微生物学报, 2025 , 65 (8) : 3782 -3793 . DOI: 10.13343/j.cnki.wsxb.20250119
Jinlu ZHU, Zeren PENG, Hongkun ZHUANG, Jie SUN, Zongfu WU. A multiplex PCR method for identification of virulent strains of Streptococcus suis serotype 4[J]. Acta Microbiologica Sinica, 2025 , 65 (8) : 3782 -3793 . DOI: 10.13343/j.cnki.wsxb.20250119
正文
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猪链球菌(Streptococcus suis)是世界范围内猪链球菌病的主要病原体，可引起猪的败血症、脑膜炎和猝死，对养猪业造成严重的经济损失[1]。此外，该菌还是一种人兽共患病原体，对与感染猪或猪肉密切接触的人群构成潜在威胁，对公共卫生构成严重威胁[2]。猪链球菌血清型众多，基于荚膜多糖抗原的差异可分为29个传统血清型(1-19、21、23-25、27-31、1/2)[3]。此外，基于荚膜基因簇的差异，近年来发现了Chz血清型和33种新荚膜基因簇菌株(NCL1-21a，21b-32)[4-6]。截至目前，已有11个血清型被报道可引起人类感染，包括血清1、2、4、5、7、9、14、16、21、24和31型[7-8]。
猪链球菌不同的血清型在种群结构和致病性方面表现出不同的特征[9-11]。流行病学监测数据显示，猪链球菌血清4型(SS4)的致病性备受关注，且该血清型还可感染人类[12-15]。本课题组最近研究发现SS4种群具有显著的多样性，最小核心基因组(minimum core genome, MCG)分群可分为MCG 1、2、3、4、7-2和7-3[11]。值得注意的是，61.90%的菌株(78/126)归类于MCG 1和MCG 3，具有潜在的人兽共患风险，尤其是属于克隆复合体(clonal complexes, CCs) CC17、CC94和CC839的毒力株[11]。此外，分析SS4种群中35个重要毒力相关基因的分布，发现SS4菌株的致病表型与毒力相关基因的分布存在显著关联，其中毒力株特异性地携带了mrp、sly、ofs、sao、dltA、IdeSsuis 、igdE和tran这8个重要毒力相关基因[11,16-17]，提示这些基因可作为SS4毒力株的分子标志。进一步通过对这些毒力相关基因进行毒力株间的多序列比对，筛选出sly、igdE、tran和sao这4个基因，这些基因具有适合设计多重PCR引物的保守序列。
鉴于SS4的致病性及潜在的公共卫生威胁，有必要建立一种简便、准确鉴别SS4毒力株的方法。因此，本研究以SS4毒力株特有的毒力相关基因sly、igdE、tran和sao作为靶基因，并结合SS4血清型特异基因wzy，设计一种多重PCR方法用于SS4毒力株的准确鉴定，以期为SS4的监测和防控提供有力的技术支持。
1 材料与方法
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1.1 菌株与培养条件
本研究采用的猪链球菌菌株信息详列于表1，菌株均由本实验室保存。其中包括SS4毒力株ND90、WUSS406、2018WUSS011、ID36054、2021WUSS075、2018WUSS156、WUSS346、2018WUSS160，弱毒株2018WUSS056、2020WUSS059、2022WUSS018、2022WUSS019、2022WUSS056、2022WUSS141、WUSS309、WUSS399，其毒力已在先前的研究中通过动物感染试验得以确认[11]。菌株ND90由中国疾病预防控制中心郑翰博士惠赠，菌株ID36054由泰国Kasetsart大学Anusak Kerdsin博士惠赠，其余菌株均由本课题组分离。在本研究中，所有菌株均在含有5%无菌绵羊血的Todd Hewitt Broth (THB)培养基平板上，于37 ℃、5% CO2条件下进行划线培养。随后，将单菌落转移至THB液体培养基中，在37 ℃、180 r/min条件下培养。
1.2 主要试剂
THB培养基购自青岛高科技工业园海博生物技术有限公司；DNA聚合酶预混液(Rapid Taq Plus DNA Polymerase)购自南京诺唯赞生物科技股份有限公司；细菌基因组DNA提取试剂盒购自普洛麦格(北京)生物技术有限公司。
1.3 靶基因序列分析及引物设计
选取毒力相关基因sly、igdE、tran和sao作为多重PCR靶基因，使用MultAlin工具(http://multalin.toulouse.inra.fr/multalin/)对不同SS4毒力株中相同毒力基因进行多序列比对以鉴定适合设计引物的保守区域。SS4血清型特异性wzy基因作为多重PCR的内参，以判断试验的有效性。靶基因序列可参考SS4毒力株ID36054基因组(登录号：CP109939.1)中sly (位点：OHM47_03295)、igdE (位点：OHM47_07760)、tran (位点：OHM47_02510)、sao (位点：OHM47_03445)和wzy (位点：OHM47_01070)。使用PrimerPlex软件设计五重PCR引物(表2)，引物均由北京擎科生物科技股份有限公司合成，浓度均为10 µmol/L。
1.4 多重PCR体系建立
1.4.1 单重PCR扩增
以表2中sly-F/R、igdE-F/R、wzy-F/R、tran-F/R和sao-F/R为引物，分别以SS4毒力株2021WUSS075和弱毒株2022WUSS056的细菌培养液(OD600=0.6)为模板进行单重PCR扩增。单重PCR扩增体系(25 μL)：Rapid Taq Plus DNA Polymerase 12.5 μL，上、下游引物(10 µmol/L)各0.75 μL，模板2.5 μL，ddH2O 8.5 μL。PCR扩增程序：95 ℃预变性5 min；98 ℃变性10 s，56 ℃退火30 s，68 ℃延伸30 s，30个循环；68 ℃终延伸5 min。PCR产物鉴定：1%琼脂糖凝胶，加样5 µL，电压180 V，电泳15 min。
1.4.2 多重PCR扩增
采用表2中的引物，上游引物和下游引物分别按照浓度1:1:1:1:1比例混合，分别以SS4毒力株2021WUSS075和弱毒株2022WUSS056的细菌培养液(OD600=0.6)为模板，进行五重PCR扩增。五重PCR扩增体系(50 μL)：Rapid Taq Plus DNA Polymerase 25 μL，上游混合引物F 7.5 μL，下游混合引物R 7.5 μL，模板5 μL，ddH2O 5 μL。PCR扩增程序：95 ℃预变性5 min；98 ℃变性10 s，56 ℃退火30 s，68 ℃延伸30 s，35个循环；68 ℃终延伸5 min。PCR产物鉴定：1%琼脂糖凝胶，加样8 µL，电压180 V，电泳20 min。
1.5 多重PCR体系的敏感性与特异性评估
按照1.4.2节中多重PCR扩增体系和扩增程序，分别以SS4毒力株2021WUSS075的细菌培养液(8.2×102-8.2×107 CFU/mL)和基因组DNA (0.025 pg/µL-2.500 ng/µL)为模板，进行五重PCR扩增，检测多重PCR体系的敏感性。Murray等[18]的研究揭示了10个猪链球菌的致病谱系，并指出其中血清1、1/2、2、3、5、6、7、8、9及14型与疾病相关且广泛流行。因此，在针对猪链球菌不同血清型特异性评估试验中，选择了这10种血清型的菌株作为对照株，菌株信息详见表1。此外，在针对非猪链球菌特异性评估试验中，以大肠杆菌(Escherichia coli)、副猪格拉菌(Glaesserella parasuis)、胸膜肺炎放线杆菌(Actinobacillus pleuropneumoniae)、金黄色葡萄球菌(Staphylococcus aureus)、肠球菌属(Enterococcus spp.)、巴氏链球菌(Streptococcus pasteurianus)、马链球菌兽疫亚种(Streptococcus equi subsp. zooepidemicus)以及无乳链球菌(Streptococcus agalactiae)作为对照株进行检测。
1.6 临床菌株多重PCR检测及斑马鱼毒力试验
采用表2中的引物，按照1.4.2节中多重PCR方法对实验室新分离的SS4菌株进行毒力株的多重PCR鉴定，并进行斑马鱼毒力试验。动物感染实验在南京农业大学实验动物中心进行[许可证号：SYXK(苏)2021-0086]。斑马鱼毒力试验参考文献[11,19-20]中描述的方法，在细菌对数生长期中期收集菌体，使用PBS洗涤2次，然后调整至适当的感染浓度。每个实验组包含15条斑马鱼，每条鱼感染剂量为3×106 CFU，记录从感染后12-96 h的死亡率。在动物感染实验中，设置猪链球菌血清2型毒力株SC070731[21]、猪链球菌血清9型无毒株SH040917[22]，以及等体积的PBS作为对照。
2 结果与分析
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2.1 靶基因选择及PCR扩增
如图1所示，比对8株毒力株(ND90、WUSS406、2018WUSS011、ID36054、2021WUSS075、2018WUSS156、WUSS346、2018WUSS160)和8株弱毒株(2018WUSS056、2020WUSS059、2022WUSS018、2022WUSS019、2022WUSS056、2022WUSS141、WUSS309、WUSS399)的毒力相关基因分布，毒力株相较于弱毒株，特异性地携带有mrp、sly、ofs、sao、dltA、IdeSsuis 、igdE和tran这8个毒力相关基因。进一步对这些毒力基因进行多序列比对后，筛选出sly、igdE、tran和sao这4个基因，它们具有适合设计多重PCR引物的保守序列。因此，选择这4个毒力相关基因，并结合SS4血清型特异性wzy基因作为多重PCR的内参，建立多重PCR方法。
采用表2中的引物，针对靶基因sly、igdE、wzy、tran和sao进行了单重PCR和五重PCR扩增。首先，以SS4毒力株2021WUSS075的细菌培养液为模板进行扩增。如图2A所示，单重PCR扩增针对这5个靶基因均成功获得了预期大小且具有特异性的PCR产物，泳道1-5分别对应基因sao (208 bp)、tran (453 bp)、wzy (604 bp)、igdE (840 bp)和sly (1 048 bp)。在五重PCR的结果中，泳道6观察到了5种预期大小的PCR产物，它们自上而下分别对应基因sly、igdE、wzy、tran和sao。相比之下，以SS4弱毒株2022WUSS056的细菌培养液为模板进行扩增。如图2B所示，在单重PCR和五重PCR扩增中，仅内参基因wzy产生了预期大小的PCR产物，其余靶基因均未产生PCR产物。这些结果表明，本研究设计的引物具有高度的特异性，能够准确地扩增出目标基因。同时，通过五重PCR方法能够有效区分SS4毒力株与弱毒株。
2.2 五重PCR体系敏感性和特异性评估
如图3所示，在多重PCR检测敏感性评估试验中，以SS4毒力株2021WUSS075的细菌培养液(浓度范围为8.2×102-8.2×107 CFU/mL)和基因组DNA (浓度范围为0.025 pg/µL至2.5 ng/µL)为模板，进行五重PCR扩增。结果显示，该五重PCR体系的最低检测限度为4.1×102 CFU菌落数(图3A，泳道4)和12.5 pg的基因组DNA (图3B，泳道4)。在多重PCR特异性评估试验中，不同血清型菌株的扩增结果呈现差异。如图3C所示，血清1、2、14型菌株的扩增产物包含4条特异性条带，自上而下分别对应毒力基因sly、igdE、tran和sao。血清1/2、3、7、9型菌株的扩增产物仅显示2条条带，对应基因igdE和sao。血清型5、6、8菌株未观察到任何扩增产物。血清型4菌株特异性扩增出5条条带，且为唯一呈现全部5种目标条带的血清型。此外，以大肠杆菌、副猪格拉菌、胸膜肺炎放线杆菌、金黄色葡萄球菌、肠球菌属、巴氏链球菌、马链球菌兽疫亚种以及无乳链球菌作为对照菌株进行检测，结果显示所有对照菌株均未出现特异性扩增产物(图3D)。上述结果表明，本研究所建立的多重PCR方法对SS4毒力株具有高度特异性，能够通过独特的5条扩增条带与其他血清型菌株明确区分，验证了该方法在血清4型鉴定中的可靠性和特异性。
2.3 鉴定新分离SS4菌株
用建立的多重PCR检测临床分离的6株SS4菌株，如图4所示，菌株ZJWUSS044、SZWUSS047和SZWUSS048扩增出5个基因，归为毒力株；而菌株SZWUSS010、SZWUSS0137和SZWUSS0138仅扩增出内参基因wzy，其余靶基因均未检测到，归为弱毒株。
2.4 斑马鱼毒力试验
斑马鱼毒力试验显示，3株经多重PCR鉴定为毒力株的ZJWUSS044、SZWUSS047、SZWUSS048对斑马鱼致病性较强，斑马鱼死亡率分别为86.67%、86.67%、60.00%；3株经多重PCR鉴定为弱毒株的SZWUSS010、SZWUSS0137和SZWUSS0138对斑马鱼致病性较低，死亡率分别为0、0和6.67% (表3)。这表明该方法可较为准确鉴定SS4毒力株。
3 讨论与结论
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猪链球菌存在多种致病血清型，大多数研究仍主要集中在血清2型，而其他致病血清型的研究相对较少。近年来的研究表明，猪链球菌血清4型(SS4)的致病性及其流行病学特征正日益受到关注。全球多国监测数据显示，SS4已呈现出显著的地域性流行趋势。在中国、韩国和加拿大，SS4在发病猪中的检出率排名第三，分别占临床分离株的5.6%-5.9%[1,23]；德国在1996-2004年和2015-2016年的2次调查中，SS4的占比均超过10%[12]。值得注意的是，动物感染模型揭示了该血清型具有强致病潜力，66.67%的SS4代表菌株对斑马鱼的致死率超过50%，且35%的猪源分离株对小鼠的致病性与人源SS4致病株ID36054相当[11]。这些证据表明，SS4不仅在全球养猪业中持续构成威胁，而且作为一种潜在的人兽共患病风险源，需要加强对其的监测。
猪链球菌能够产生多种毒力相关因子，不同菌株中这些因子的种类和数量存在差异。前期研究发现，SS4毒力株特异性地携带有sly、igdE、tran和sao这4个在致病过程中具有重要作用的毒力相关基因。这些基因分别编码溶血素(suilysin, Sly)、猪链球菌免疫球蛋白G分解酶(IgdE)、表面蛋白Sao和转录调控因子Tran，它们在猪链球菌的致病机制中发挥着重要作用。Sly是一种由猪链球菌产生的胆固醇依赖性穿孔毒素，在猪链球菌的致病过程中发挥关键作用，被广泛认为是该菌毒力的关键标志物[24]。Sly通过在宿主细胞膜上形成孔洞，导致细胞裂解，对多种细胞类型具有广泛的细胞毒性作用，包括上皮细胞、内皮细胞和免疫细胞[25-27]。此外，Sly还能影响宿主的补体系统，有助于猪链球菌的免疫逃避，并可能改变宿主的血脑屏障，促进病原菌诱导脑膜炎等疾病[24,28]。IgdE对IgG具有蛋白水解活性，且对猪IgG显示出高度特异性，表明IgdE可能是一种新型且重要的毒力相关因子[29]。Sao蛋白在猪链球菌中高度保守，是一种表面蛋白，不仅存在于血清2型菌株中，也在多种致病性血清型中广泛分布[30]。Sao还能够诱导宿主产生强烈的免疫反应，因此常被选作疫苗设计的候选蛋白以及诊断猪链球菌感染的标志物[31-32]。转录调节因子Tran参与猪链球菌细胞代谢和应激耐受，调控多种毒力相关因子[17,33]。基因tran缺失会导致130个基因的表达发生变化，对环境应激的耐受性下降，与上皮细胞的黏附能力减弱，并且在斑马鱼模型中的毒力显著降低，表明Tran是猪链球菌致病性的一个关键调控因子[33]。此外，在前期的研究中，对126个SS4基因组中重要毒力相关基因的分布情况进行了系统分析。研究表明，sly、igdE、sao和tran与其他关键毒力相关基因存在显著的连锁特征：携带这4个毒力相关基因的SS4毒力株同时具有多个重要的毒力相关基因，包括ef、mrp、ofs、IdeSsuis 、sbp2、dltA、hp0197、hp0272和rgg[11]。值得注意的是，其中mrp、IdeSsuis 、sbp2、hp0197、hp0272和rgg基因已被证实具有人兽共患潜能[34]。综上所述，sly、igdE、sao和tran这4种毒力基因因其重要的致病作用和在SS4毒力株中的特异性携带，适合作为鉴定SS4毒力株的靶基因。
本研究的特异性试验结果显示，部分非SS4血清型菌株能够扩增出全部或部分毒力基因条带。这一现象可能与不同血清型中毒力基因的保守性差异有关。例如，毒力基因sly和sao不仅存在于血清2型菌株中，还广泛分布于多种具有致病性的血清型[30,35]。本研究中某些血清1、2、14型菌株的4种毒力基因均呈阳性，提示这些菌株可能具有毒力。然而，毒力相关基因的表达水平可能会因血清型背景的差异而有所不同[36]。因此，这些基因是否也可作为其他血清型毒力株的鉴定标准，仍需进一步验证。因此，为了更有效地区分SS4毒力株与其他血清型的菌株，本研究建立的多重PCR方法采用了“4+1”基因组合(4个毒力基因+1个血清型特异性基因)。通过这种组合，能够有效地将SS4毒力株与其他血清型菌株区分开来。
综上所述，本研究基于SS4毒力株特有的毒力相关基因sly、igdE、tran和sao作为靶基因，并结合SS4血清型特异性wzy基因，成功开发了一种SS4毒力株鉴别的五重PCR方法，可准确、简便地鉴定SS4毒力株，为SS4的监测和防控提供有力的技术支持。
基金
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  • 国家重点研发计划(2023YFD1800503)
  • 深圳市科技计划(KCXFZ20230731094003006)
文献
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参考文献 引证文献
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2025年第65卷第8期
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doi: 10.13343/j.cnki.wsxb.20250119
  • 接收时间：2025-02-19
  • 首发时间：2026-02-06
  • 出版时间：2025-08-04
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  • 收稿日期：2025-02-19
  • 录用日期：2025-03-19
基金
National Key Research and Development Program of China(2023YFD1800503)
国家重点研发计划(2023YFD1800503)
Shenzhen Science and Technology Program(KCXFZ20230731094003006)
深圳市科技计划(KCXFZ20230731094003006)
作者信息
    1.南京农业大学 动物医学院，江苏 南京
    2.农业部动物细菌学重点实验室，江苏 南京
    3.世界动物卫生组织猪链球菌病参考实验室，江苏 南京
    4.深圳海关动植物检验检疫技术中心，广东 深圳
    5.广东省养猪与猪病防控技术研究企业重点实验室，广东海大畜牧兽医研究院，广东 广州

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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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