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Article(id=1241045261619876161, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1239895163967959761, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20230213, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1680105600000, receivedDateStr=2023-03-30, revisedDate=null, revisedDateStr=null, acceptedDate=1695744000000, acceptedDateStr=2023-09-27, onlineDate=1773817847875, onlineDateStr=2026-03-18, pubDate=1704297600000, pubDateStr=2024-01-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773817847875, onlineIssueDateStr=2026-03-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773817847875, creator=13701087609, updateTime=1773817847875, updator=13701087609, issue=Issue{id=1239895163967959761, tenantId=1146029695717560320, journalId=1192105938417971205, year='2024', volume='64', issue='1', pageStart='1', pageEnd='322', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1773543643228, creator=13701087609, updateTime=1773820020328, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241054373594320900, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1239895163967959761, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241054373598515205, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1239895163967959761, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=108, endPage=129, ext={EN=ArticleExt(id=1241045262118998353, articleId=1241045261619876161, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Comparative transcriptomics ofBacillus thuringiensis Bt4.0718 reveals the mechanisms of sporulation and parasporal crystal formation, columnId=1241045257748533520, journalTitle=Acta Microbiologica Sinica, columnName=Research Articles, runingTitle=null, highlight=null, articleAbstract=

[Objective] Bacillus thuringiensis (Bt), characterized by the massive production of insecticidal crystal proteins (ICPs) during sporulation, serves as the main strain resource for the commonly used and safe microbial insecticides. To further explore the mechanisms of sporulation and parasporal crystal formation and lay a theoretical foundation for the construction of efficient strains, we compared the transcriptomes of Bt at three important stages.[Methods] The transcriptomes of the hypervirulent strain Bt4.0718 at the middle vegetative growth stage (T1-10 h), the early sporulation stage (T2-20 h), and the late sporulation stage (T3-32 h) were compared. The representative differentially expressed genes (DEGs) were verified by real-time fluorescence quantitative PCR (qRT-PCR), and the phenotypes of the mutant strains with the knockout of specific functional genes were examined.[Results] The number of DEGs was 2 147 (T2/T1), 1 861 (T3/T1), and 1 708 (T3/T2), respectively. At T1, the medium was rich in nutrients, which served the sporulation and parasporal crystal formation. The high transcription levels ofkinA/D,spo0A/F, andsigE regulating sporulation played a role in the growth and development of the cells. The transcription of Cry1Ac, poly-hydroxybutyric acid (PHB), and hydroxybutanone (acetoin) were started at this time. The substantial formation of ICPs and spores occurred at T2 and T3, and the transcript levels of the regulatory genes were higher at T2 than those at T3. The genes associated with spore core/coat/cortex, germination protein, andspoII–spoVI began to be transcribed in large amounts at T2, with the highest levels among the three stages. The corresponding complex networks of carbohydrate, amino acid, and lipid metabolism, energy, nucleic acid, and peptide metabolism, secondary metabolite production, and environmental adaptation showed differences. In addition, as the physiological processes stimulated by nutrient signals, the two-component signal transduction system (TCS) and ABC transport system played an essential role in the process of sporulation and ICP transcription and expression, and their transcription levels were significantly different.[Conclusion] With the production of ICPs and sporulation, nutrients are gradually consumed, and the high expression ofsigB,sigW, andsigM contributed to the stability of cell wall and the resistance to environmental changes. Meanwhile, the small heat shock proteins Hsp20 and Hsp20B, as molecular chaperones, were also important for maintaining intracellular homeostasis and may facilitate the sporulation and ICP production.

, correspAuthors=Xuezhi DING, authorNote=null, correspAuthorsNote=
*DING Xuezhi, E-mail:
, copyrightStatement=Copyright ©2024 Acta Microbiologica Sinica. All rights reserved., copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=Junyan XIE, Sisi LUO, Zirong ZHU, Wenhui CHEN, Kexuan ZHOU, Liqiu XIA, Xuezhi DING), CN=ArticleExt(id=1241045271942058611, articleId=1241045261619876161, tenantId=1146029695717560320, journalId=1192105938417971205, language=CN, title=苏云金杆菌Bt4.0718不同时期比较转录组揭示芽胞和杀虫伴胞晶体形成机制, columnId=1192149544164012138, journalTitle=微生物学报, columnName=研究报告, runingTitle=null, highlight=null, articleAbstract=

【目的】苏云金芽胞杆菌(Bacillus thuringiensis, Bt)在形成芽胞的过程中产生大量杀虫晶体蛋白(insecticidal crystal proteins, ICPs)，是目前应用最广泛、最安全的微生物杀虫剂的主要菌株资源。本研究旨在比较Bt 3个重要时期的转录组，进一步探究芽胞和杀虫伴胞晶体的形成机制，为高效工程菌的构建奠定理论基础。【方法】选取高毒力Bt4.0718菌株营养生长中期(T1-10 h)、芽胞形成前期(T2-20 h)、芽胞形成后期(T3-32 h)进行比较转录组分析，对代表性差异基因进行实时荧光定量PCR (real-time fluorescence quantitative PCR, qRT-PCR)验证、特定功能基因的敲除和表型分析验证。【结果】差异表达基因数量分别为2 147个(T2/T1)、1 861个(T3/T1)、1 708个(T3/T2)。T1时期，培养基中营养相对丰富，主要为芽胞和杀虫伴胞晶体形成做准备。芽胞形成重要调控基因kinA/D、spo0A/F、sigE高水平转录对菌体的生长发育具有重要作用，Cry1Ac、碳源、能源贮藏物聚-羟基丁酸(poly-hydroxybutyric acid, PHB)和羟基丁酮(acetoin)也已开始转录。芽胞和ICPs的大量形成在T2和T3时期，相关基因的转录水平T2比T3时期高。T2对比T3时期，芽胞核/衣/皮质(spore core/coat/cortex)、芽胞萌发受体蛋白(germination protein)和芽胞形成的Ⅱ−Ⅵ阶段相关基因(spoⅡ−spoⅥ)在T2时才开始大量转录，为3个时期的最高水平；相应的糖类、氨基酸、脂质代谢，能量、核酸、多肽代谢、次级产物生成和环境适应系统等复杂网络均表现出差异；另外，作为营养信号刺激性生理过程，双组分信号转导系统(two-component signal transduction system, TCS)和ABC转运系统在芽胞形成和ICPs的转录表达过程中发挥重要作用，转录水平具有显著差异。【结论】随着芽胞和杀虫伴胞晶体的形成，营养成分逐渐匮乏，sigB、sigW和sigM的高效表达有助维持细胞壁的稳定和对环境变化的抗性；小热激蛋白Hsp20和Hsp20B作为分子伴侣蛋白对维持胞内稳态也十分重要，T2、T3时期高水平转录可能有助于芽胞形成和ICPs表达。

, correspAuthors=丁学知, authorNote=null, correspAuthorsNote=null, copyrightStatement=版权所有©《微生物学报》编辑部2024, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=xZ0UqAmXUprvnkyezs1Chg==, magXml=AtHzqLioxmlGwiBJobxcqg==, pdfUrl=null, pdf=ejociRJIAi4cZ6oXfBeOQw==, pdfFileSize=1567365, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=5EkshTajH8nINO60sql4Rw==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=p9keWjV+WQeVKmIFmbQo2g==, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=谢俊雁, 罗斯思, 朱梓榕, 陈文慧, 周客轩, 夏立秋, 丁学知)}, authors=[Author(id=1241084438856127301, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, orderNo=0, firstName=null, middleName=null, lastName=null, nameCn=null, orcid=null, stid=null, country=null, authorPic=null, dead=0, email=null, emailSecond=null, emailThird=null, correspondingAuthor=0, authorType=1, ext={EN=AuthorExt(id=1241084438994539341, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, authorId=1241084438856127301, language=EN, stringName=Junyan XIE, firstName=Junyan, middleName=null, lastName=XIE, prefix=null, suffix=null, authorComment=null, nameInitials=null, affiliation=null, department=null, xref=1, 2, address=1 Hunan Provincial Key Laboratory of Microbial Molecular Biology, State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal University, Changsha 410081, Hunan, China
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A: T1, logarithmic phase. B: T2, pre-sporulation period. C: T3, late stage of sporulation. 1: Spore; 2: Parasporal crystal., figureFileSmall=hHzPNqA+Hc5m1RaazkqC4Q==, figureFileBig=pZhdbS3fmEEV30y59q/3Tg==, tableContent=null), ArticleFig(id=1241084444006731796, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图1, caption=Bt4.0718发酵培养不同时间相差显微观察, figureFileSmall=hHzPNqA+Hc5m1RaazkqC4Q==, figureFileBig=pZhdbS3fmEEV30y59q/3Tg==, tableContent=null), ArticleFig(id=1241084444128366615, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 2, caption=PCA analysis of transcriptome samples at different periods., figureFileSmall=W2uY1WlDKGfsJRcA6EJang==, figureFileBig=DLCDaZ96c5GbqCXzZQORNQ==, tableContent=null), ArticleFig(id=1241084444216447007, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图2, caption=转录组不同时期样品的PCA分析, figureFileSmall=W2uY1WlDKGfsJRcA6EJang==, figureFileBig=DLCDaZ96c5GbqCXzZQORNQ==, tableContent=null), ArticleFig(id=1241084444321304612, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 3, caption=Venn diagrams (A) and the number of differential genes statistics (B) which compared three periods., figureFileSmall=slTPjTXCj+lNYQlOT8Bd1g==, figureFileBig=Gxgm7TWMER0lVYns/xbDRg==, tableContent=null), ArticleFig(id=1241084444413579303, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图3, caption=三个重要时期转录组韦恩图(A)和差异基因统计(B), figureFileSmall=slTPjTXCj+lNYQlOT8Bd1g==, figureFileBig=Gxgm7TWMER0lVYns/xbDRg==, tableContent=null), ArticleFig(id=1241084444526825516, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 4, caption=Results of qRT-PCR ofcry1Ac,cry2Aa,sigK, andcwlD genes at different periods. Data were shown as the mean of three replicates, with the error bars representing±standard error., figureFileSmall=057CjJW6FXGvciyFn8AgUQ==, figureFileBig=duVTvKRDd5aE5k8juLVx8w==, tableContent=null), ArticleFig(id=1241084444606517292, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图4, caption=不同时期cry1Ac、cry2Aa、sigK、cwlD基因的qRT-PCR结果, figureFileSmall=057CjJW6FXGvciyFn8AgUQ==, figureFileBig=duVTvKRDd5aE5k8juLVx8w==, tableContent=null), ArticleFig(id=1241084444686209074, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 5, caption=Verification results of qRT-PCR of other up-down-regulated genes in the transcriptome at different periods. A: Results of qRT-PCR ofhsp20B,leuB,lysA,hsp20,glnA,phoR, andspo0A genes at different periods. B: Results of qRT-PCR ofpyrG,guaB,hemE,odhB,groeL,glyA,pgk, andhslV genes at different periods. Data were shown as the mean of three replicates, with the error bars representing±standard error., figureFileSmall=D4/oiBKwSiy5m8jYCGmNLw==, figureFileBig=3Slzb7Z00zAvXr/j07KHzA==, tableContent=null), ArticleFig(id=1241084444757512246, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图5, caption=不同时期转录组中其他上下调基因的qRT-PCR验证结果, figureFileSmall=D4/oiBKwSiy5m8jYCGmNLw==, figureFileBig=3Slzb7Z00zAvXr/j07KHzA==, tableContent=null), ArticleFig(id=1241084446275850300, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 6, caption=Venn diagram of significantly differential genes., figureFileSmall=QRHZ9elhm7F8sUtseZe1Bg==, figureFileBig=gQzmHLhylGXN3Ajq9eENGQ==, tableContent=null), ArticleFig(id=1241084446368124995, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图6, caption=三组显著差异基因韦恩图, figureFileSmall=QRHZ9elhm7F8sUtseZe1Bg==, figureFileBig=gQzmHLhylGXN3Ajq9eENGQ==, tableContent=null), ArticleFig(id=1241084446456205380, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 7, caption=KEGG analysis result of the differential genes in regions Ⅰ (A) and Ⅱ (B)., figureFileSmall=9nflq1KENDXgpkifzNwcbg==, figureFileBig=EoH3lX8Yco60f/TCPsjlZA==, tableContent=null), ArticleFig(id=1241084446561062984, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图7, caption=Ⅰ (A)和Ⅱ (B)号区域差异基因KEGG分析结果, figureFileSmall=9nflq1KENDXgpkifzNwcbg==, figureFileBig=EoH3lX8Yco60f/TCPsjlZA==, tableContent=null), ArticleFig(id=1241084446682697808, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 8, caption=KEGG analysis result of the differential genes in regions Ⅳ (A) and Ⅴ (B)., figureFileSmall=fctEvw8KTxFkFa/9ZRMSEQ==, figureFileBig=obPkOvA1J0+kTnxnVhzwUw==, tableContent=null), ArticleFig(id=1241084446825304148, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图8, caption=Ⅳ (A)和Ⅴ (B)号区域差异基因KEGG分析结果, figureFileSmall=fctEvw8KTxFkFa/9ZRMSEQ==, figureFileBig=obPkOvA1J0+kTnxnVhzwUw==, tableContent=null), ArticleFig(id=1241084446900801626, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 9, caption=KEGG analysis result of the differential genes in regions Ⅵ (A) and Ⅶ (B)., figureFileSmall=tD7WP0pbSd+Ul0n81NreLw==, figureFileBig=AvFMo+21SDjFjoon4R8Cmg==, tableContent=null), ArticleFig(id=1241084446980493405, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图9, caption=Ⅵ (A)和Ⅶ (B)号区域差异基因KEGG分析结果, figureFileSmall=tD7WP0pbSd+Ul0n81NreLw==, figureFileBig=AvFMo+21SDjFjoon4R8Cmg==, tableContent=null), ArticleFig(id=1241084447085351009, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 10, caption=Time cluster analysis results., figureFileSmall=ufRFqbmrWaPR/T/3pSNw9w==, figureFileBig=ZcKWhOF6JZYkrm5zY90Byg==, tableContent=null), ArticleFig(id=1241084447194402917, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图10, caption=时间序列分析结果, figureFileSmall=ufRFqbmrWaPR/T/3pSNw9w==, figureFileBig=ZcKWhOF6JZYkrm5zY90Byg==, tableContent=null), ArticleFig(id=1241084447274094699, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 11, caption=KEGG analysis result of cluster 2., figureFileSmall=g9yn7nC8O7sNTKHSaeKdqw==, figureFileBig=IfWdDMhKKL7xpN1JF7sJDQ==, tableContent=null), ArticleFig(id=1241084447345397871, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图11, caption=Cluster 2基因簇KEGG分析结果, figureFileSmall=g9yn7nC8O7sNTKHSaeKdqw==, figureFileBig=IfWdDMhKKL7xpN1JF7sJDQ==, tableContent=null), ArticleFig(id=1241084447433478260, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 12, caption=KEGG analysis results of cluster 7., figureFileSmall=cta3G91MFUiDoS9iZQGV6g==, figureFileBig=99ipMm+gUte7A63EKfhs/g==, tableContent=null), ArticleFig(id=1241084447513170041, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图12, caption=Cluster 7基因簇KEGG分析, figureFileSmall=cta3G91MFUiDoS9iZQGV6g==, figureFileBig=99ipMm+gUte7A63EKfhs/g==, tableContent=null), ArticleFig(id=1241084447626416252, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 13, caption=Identification ofhsp20 knockout. Identification of PCR amplifies. Lane 1: Wild type strain; Lane 2: Complemented strain; Lanes 3−4: Knockout strain; Lanes 5−6: 16S rRNA gene sequence of wild type and knockout strain., figureFileSmall=BNrqSTPnQMQCwBLj+Io07A==, figureFileBig=uND5TsIDEHxHB2X00OThCA==, tableContent=null), ArticleFig(id=1241084447735468160, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图13, caption=hsp20基因敲除鉴定, figureFileSmall=BNrqSTPnQMQCwBLj+Io07A==, figureFileBig=uND5TsIDEHxHB2X00OThCA==, tableContent=null), ArticleFig(id=1241084447823548548, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 14, caption=Growth curves of the Bt 4.0718, Bt4-∆hsp20, and Bt4-∆hsp20: :hsp20 strains in fermentation medium. Data were shown as the mean of three replicates, with the error bars representing±standard error., figureFileSmall=ztBonM3hUBiYE625zGusPQ==, figureFileBig=4c0E9POqdaKaB2v0vxg7/g==, tableContent=null), ArticleFig(id=1241084447890657417, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图14, caption=Bt4.0718原始菌株及其hsp20敲除和回复菌株发酵培养基的生长曲线, figureFileSmall=ztBonM3hUBiYE625zGusPQ==, figureFileBig=4c0E9POqdaKaB2v0vxg7/g==, tableContent=null), ArticleFig(id=1241084447961960590, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Figure 15, caption=Analysis of sporulation and parasporal crystal formation in Bt4-∆hsp20. A: Phase contrast microscopy of the strains at 12 h, 24 h, and 36 h, and the scanning electron microscopy of the spores and parasporal crystals (10 000×) at 36 h. B: Sporulation of the Bt4-∆hsp20 compared to Bt4.0718, and Bt4-∆hsp20: :hsp20 strains in LB at 60 h (CFU/mL), and each experiment was carried out in triplicate, significances of differences by Student'st-test was indicated. **:P≤0.01. C: ICPs in Bt4.0718 and Bt4-∆hsp20 strains at 20 h analyzed by SDS-PAGE. D: Concentrations of ICPs at 20 h determined by Bradford method in Bt4-∆hsp20 compared to Bt4.0718, and Bt4-∆hsp20: :hsp20 strains, the significances of differences by Student'st-test was indicated. **:P≤0.01. E: qRT-PCR analysis the fold change ofcry1Ac andcry1Aa in Bt4-∆hsp20 strain which compared to Bt4.0718 after fermentation for 28 h, the significances of differences by Student'st-test were indicated. *:P≤0.05. Data were shown as the mean of three replicates, with the error bars representing±standard error., figureFileSmall=rvS5/z4sIwiecAzmU+Td5Q==, figureFileBig=7Wc0uMVmcWoY/hK7n6yF8w==, tableContent=null), ArticleFig(id=1241084448024875154, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=图15, caption=Bt4-∆hsp20菌株显微观察及芽胞和伴胞晶体形成能力分析, figureFileSmall=rvS5/z4sIwiecAzmU+Td5Q==, figureFileBig=7Wc0uMVmcWoY/hK7n6yF8w==, tableContent=null), ArticleFig(id=1241084448121344149, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 1, caption=

primers for qRT-PCR

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PrimersSequence (5ʹ→3ʹ)
cry1Ac-qFATATTTCCTTGTCGCTAACGCA
cry1Ac-qRTGTACAAGAAATGCGTCCCATT
cry2Aa-qFCCCTTGCTCGTGTAAATGCA
cry2Aa-qRAGGAACAGGGTTTTGAGTAGGG
cwlD-qFTATCAGGGAAAGTAATTGTATTAGATGC
cwlD-qRGCACCTTGTTCTTGTAAATAGTCTTGT
sigK-qFATCGGGCAAGATAAAGAGGGTA
sigK-qRCTCCTTATCTAGCCCAAGTCCAA
groeL-qFGATCAATTTGGTCATGCTGGTG
groeL-qRCGGAGCATTTGGATCACGAC
glnA-qFACTTCAATCTTGGACCAGAGCC
glnA-qRCGAAGTATCCACCGTTATCGTTTAG
glyA-qFAGGCAGAACTAGGAAGACAGCG
glyA-qRACAGAACCTTGTGCCTCCATTAC
guaB-qFTGATATGCGCTTCATCCAAGAC
guaB-qRACCGTTATTATCAACAAGAGGGAGT
hemE-qFCAATATAACGTAGACGCAGCAATTCT
hemE-qRCATCTTCTGGATTGATTTCCCCTA
hsp20-qFTGCTTTCTTGAAGCCACTGAAC
hsp20-qRAACCTGGTAAATCTGCTTTCACAGT
hsp20B-qFTCTTCGCAATGTAATCGCTGAT
hsp20B-qRCAACGAGTTCTTCACCAACTTCAT
hslV-qFATCCGGTTCAATTACTTCTCCTG
hslV-qRCAGTTGCTGACGCATTTACTCTTT
leuB-qFACCCAAATGTGGAAGTAGAACACA
leuB-qRCGTGAATAGGCTCGTATAATGAAGG
lysA-qFGAAATAGTGATGGCTCTTCAGGC
lysA-qRGAATCATCTTGGCCTGTCGTAAT
odhB-qFGGTTACCAAATACAAACCGTCCTA
odhB-qRCGTCCAAGTGGGTCTGTGCTA
phoR-qFCATGCGGTGTTCGTTCAAGA
phoR-qRCAACTACGAGACAAGCAATGACAA
pyrG-qFAGATGATGGCGCAGAAACTGAC
pyrG-qRCCTAAATATTCACCGCGACGC
pgk-qFGCATCTGCTAATGCTTGTCCTACT
pgk-qRTCTAACTGGGAAGGCGTGGA
spo0A-qFCGTCCACTACCATCATTCCGA
spo0A-qFAGCGGGTACACCAATTTCATG
16S-qFAGAGTTTGATCCTGGCTCAG
16S-qRACGGCTACCTTGTTACGACTT
), ArticleFig(id=1241084448222007451, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表1, caption=

qRT-PCR验证引物

, figureFileSmall=null, figureFileBig=null, tableContent=
PrimersSequence (5ʹ→3ʹ)
cry1Ac-qFATATTTCCTTGTCGCTAACGCA
cry1Ac-qRTGTACAAGAAATGCGTCCCATT
cry2Aa-qFCCCTTGCTCGTGTAAATGCA
cry2Aa-qRAGGAACAGGGTTTTGAGTAGGG
cwlD-qFTATCAGGGAAAGTAATTGTATTAGATGC
cwlD-qRGCACCTTGTTCTTGTAAATAGTCTTGT
sigK-qFATCGGGCAAGATAAAGAGGGTA
sigK-qRCTCCTTATCTAGCCCAAGTCCAA
groeL-qFGATCAATTTGGTCATGCTGGTG
groeL-qRCGGAGCATTTGGATCACGAC
glnA-qFACTTCAATCTTGGACCAGAGCC
glnA-qRCGAAGTATCCACCGTTATCGTTTAG
glyA-qFAGGCAGAACTAGGAAGACAGCG
glyA-qRACAGAACCTTGTGCCTCCATTAC
guaB-qFTGATATGCGCTTCATCCAAGAC
guaB-qRACCGTTATTATCAACAAGAGGGAGT
hemE-qFCAATATAACGTAGACGCAGCAATTCT
hemE-qRCATCTTCTGGATTGATTTCCCCTA
hsp20-qFTGCTTTCTTGAAGCCACTGAAC
hsp20-qRAACCTGGTAAATCTGCTTTCACAGT
hsp20B-qFTCTTCGCAATGTAATCGCTGAT
hsp20B-qRCAACGAGTTCTTCACCAACTTCAT
hslV-qFATCCGGTTCAATTACTTCTCCTG
hslV-qRCAGTTGCTGACGCATTTACTCTTT
leuB-qFACCCAAATGTGGAAGTAGAACACA
leuB-qRCGTGAATAGGCTCGTATAATGAAGG
lysA-qFGAAATAGTGATGGCTCTTCAGGC
lysA-qRGAATCATCTTGGCCTGTCGTAAT
odhB-qFGGTTACCAAATACAAACCGTCCTA
odhB-qRCGTCCAAGTGGGTCTGTGCTA
phoR-qFCATGCGGTGTTCGTTCAAGA
phoR-qRCAACTACGAGACAAGCAATGACAA
pyrG-qFAGATGATGGCGCAGAAACTGAC
pyrG-qRCCTAAATATTCACCGCGACGC
pgk-qFGCATCTGCTAATGCTTGTCCTACT
pgk-qRTCTAACTGGGAAGGCGTGGA
spo0A-qFCGTCCACTACCATCATTCCGA
spo0A-qFAGCGGGTACACCAATTTCATG
16S-qFAGAGTTTGATCCTGGCTCAG
16S-qRACGGCTACCTTGTTACGACTT
), ArticleFig(id=1241084448335253662, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 2, caption=

Transcriptional levels of structure and composition of genes related to spore

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GeneFPKMDescription
T1T2T3
ssp71.341 814.31 835.8Acid-soluble spore protein
sspE100.774 330.110 031.3Acid-soluble spore protein
sspI8.7361.924.8Acid-soluble spore protein
sspH11.610.50.0Acid-soluble spore protein H
sspK38.720 149.7876.0Acid-soluble spore protein K
sspN0.0134.463.0Acid-soluble spore protein N
sspO16.61 613.375.7Acid-soluble spore protein O
sspP0.0139.661.1Acid-soluble spore protein P
tlp0.0333.662.1Acid-soluble spore protein
sspB11.43 268.8585.4Small acid-soluble spore protein
safA0.689.539.6Spore coat assembly factor SafA
cotD200.3252 748.913 549.4Spore coat protein
cotE12.99 788.8630.0Spore coat protein
cotF2.815.719.1Spore coat protein
cotH3.939.020.2Spore coat protein
cotM9.14 936.25 541.8Spore coat protein
cotW0.016.5254.5Spore coat protein
cotX2.6419.357 082.5Spore coat protein
cotX13.71 236.196 802.6Spore coat protein
cotZ240.1280 324.85 213.3Spore coat protein
cotC4.40.05.5Spore coat protein C
cotJB0.052.420.3Spore coat protein CotJB
cotS6.0279.590.2Spore coat protein CotS
cotG32.232 818.910 399.0Spore coat protein G
cotZ20.48 640.4451.8Spore coat protein Z
yabQ18.710.851.3Spore cortex biosynthesis protein YabQ
dapA2.82 222.4110.8Dipicolinate synthase subunit A
dapB5.93 281.5167.9Dipicolinate synthase subunit B
dapD256.164.1353.4Tetrahydrodipicolinate N-acetyltransferase
), ArticleFig(id=1241084448423334049, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表2, caption=

芽胞结构和组分相关基因转录水平

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GeneFPKMDescription
T1T2T3
ssp71.341 814.31 835.8Acid-soluble spore protein
sspE100.774 330.110 031.3Acid-soluble spore protein
sspI8.7361.924.8Acid-soluble spore protein
sspH11.610.50.0Acid-soluble spore protein H
sspK38.720 149.7876.0Acid-soluble spore protein K
sspN0.0134.463.0Acid-soluble spore protein N
sspO16.61 613.375.7Acid-soluble spore protein O
sspP0.0139.661.1Acid-soluble spore protein P
tlp0.0333.662.1Acid-soluble spore protein
sspB11.43 268.8585.4Small acid-soluble spore protein
safA0.689.539.6Spore coat assembly factor SafA
cotD200.3252 748.913 549.4Spore coat protein
cotE12.99 788.8630.0Spore coat protein
cotF2.815.719.1Spore coat protein
cotH3.939.020.2Spore coat protein
cotM9.14 936.25 541.8Spore coat protein
cotW0.016.5254.5Spore coat protein
cotX2.6419.357 082.5Spore coat protein
cotX13.71 236.196 802.6Spore coat protein
cotZ240.1280 324.85 213.3Spore coat protein
cotC4.40.05.5Spore coat protein C
cotJB0.052.420.3Spore coat protein CotJB
cotS6.0279.590.2Spore coat protein CotS
cotG32.232 818.910 399.0Spore coat protein G
cotZ20.48 640.4451.8Spore coat protein Z
yabQ18.710.851.3Spore cortex biosynthesis protein YabQ
dapA2.82 222.4110.8Dipicolinate synthase subunit A
dapB5.93 281.5167.9Dipicolinate synthase subunit B
dapD256.164.1353.4Tetrahydrodipicolinate N-acetyltransferase
), ArticleFig(id=1241084448557551779, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 3, caption=

The transcription levels of peptidoglycan related genes of spore

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GeneFPKMDescription
T1T2T3
ampC106.99.518.86-aminohexanoate-oligomer exohydrolase
cwlA57.455.142.3N-acetylmuramoyl-l-alanine amidase
cwlD2.331.97.6N-acetylmuramoyl-l-alanine amidase
cwlJ9.2598.4272.8Cell wall hydrolase
cwlO1101.574.8406.1N-acetylmuramoyl-l-alanine amidase
dacC17.157.627.7d-alanyl-d-alanine carboxypeptidase
dacF1.744.142.1d-alanyl-d-alanine carboxypeptidase
ftsI148.621.526.6Penicillin-binding protein
lysM2.86.87.1Peptigoglycan-binding protein LysM
mecA37.67.738.4Beta-lactam-resistant peptidoglycan transpeptidase
mur11.561.91 620.5N-acetylmuramoyl-l-alanine amidase
pbp1A44.18.449.0Penicillin-binding protein
pbp2D8.523.124.7Penicillin-binding protein 2D
PGPR2.74.13.4Peptidoglycan recognition proteins
sleB1.111.83.4Hydrolase, spore cortex-lytic enzyme
spoVD50.79.251.2Stage Ⅴ sporulation protein D (sporulation-specific penicillin-binding protein)
), ArticleFig(id=1241084448645632166, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表3, caption=

芽胞肽聚糖相关基因转录水平

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
ampC106.99.518.86-aminohexanoate-oligomer exohydrolase
cwlA57.455.142.3N-acetylmuramoyl-l-alanine amidase
cwlD2.331.97.6N-acetylmuramoyl-l-alanine amidase
cwlJ9.2598.4272.8Cell wall hydrolase
cwlO1101.574.8406.1N-acetylmuramoyl-l-alanine amidase
dacC17.157.627.7d-alanyl-d-alanine carboxypeptidase
dacF1.744.142.1d-alanyl-d-alanine carboxypeptidase
ftsI148.621.526.6Penicillin-binding protein
lysM2.86.87.1Peptigoglycan-binding protein LysM
mecA37.67.738.4Beta-lactam-resistant peptidoglycan transpeptidase
mur11.561.91 620.5N-acetylmuramoyl-l-alanine amidase
pbp1A44.18.449.0Penicillin-binding protein
pbp2D8.523.124.7Penicillin-binding protein 2D
PGPR2.74.13.4Peptidoglycan recognition proteins
sleB1.111.83.4Hydrolase, spore cortex-lytic enzyme
spoVD50.79.251.2Stage Ⅴ sporulation protein D (sporulation-specific penicillin-binding protein)
), ArticleFig(id=1241084448809210027, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 4, caption=

Sigma regulators in the transcriptome data

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GeneFPKMDescription
T1T2T3
bofA7.50.00.0Sigma-K factor-processing regulatory protein BofA
bofC1.754.130.3Forespore regulator of the sigma-K checkpoint
deoR14.62.937.8RNA polymerase sigma factor
raiA42 664.3613.92 058.3Sigma-54 modulation protein
rpoD1 375.8236.4736.5RNA polymerase sigma factor RpoD
rpoE9.25.013.2RNA polymerase sigma factor
sig5494.178.234.7RNA polymerase subunit sigma-54
sigB17.94.521.9RNA polymerase sigma factor SigB
sigE9.338.222.5RNA polymerase sigma factor
sigF509.4182.0372.7RNA polymerase sigma factor
sigG7.94856.03293.1RNA polymerase sigma-G factor
sigH588.321.250.7RNA polymerase sigma-H factor
sigJ19.421.413.9RNA polymerase sigma factor SigJ
sigMR11.617.622.1Sigma-M negative effector
sigW3.70.00.0RNA polymerase sigma factor SigW
sigX2.34.33.9RNA polymerase sigma factor SigX
), ArticleFig(id=1241084448926650542, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表4, caption=

转录组中sigma调控因子

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
bofA7.50.00.0Sigma-K factor-processing regulatory protein BofA
bofC1.754.130.3Forespore regulator of the sigma-K checkpoint
deoR14.62.937.8RNA polymerase sigma factor
raiA42 664.3613.92 058.3Sigma-54 modulation protein
rpoD1 375.8236.4736.5RNA polymerase sigma factor RpoD
rpoE9.25.013.2RNA polymerase sigma factor
sig5494.178.234.7RNA polymerase subunit sigma-54
sigB17.94.521.9RNA polymerase sigma factor SigB
sigE9.338.222.5RNA polymerase sigma factor
sigF509.4182.0372.7RNA polymerase sigma factor
sigG7.94856.03293.1RNA polymerase sigma-G factor
sigH588.321.250.7RNA polymerase sigma-H factor
sigJ19.421.413.9RNA polymerase sigma factor SigJ
sigMR11.617.622.1Sigma-M negative effector
sigW3.70.00.0RNA polymerase sigma factor SigW
sigX2.34.33.9RNA polymerase sigma factor SigX
), ArticleFig(id=1241084449035702450, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 5, caption=

The transcription level of sporulation genes

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GeneFPKMDescription
T1T2T3
spoIIAA218.545.675.4Anti-sigma F factor antagonist
ftsK3.049.57.0Cell division protein FtsK
rsfA58.6345.789.9Prespore-specific transcriptional regulator rsfA
gerA2.420.412.7Spore germination protein GerA
gerD163.469.39.2Spore germination protein GerD
gerQ10.0645.3392.4Spore germination protein GerQ
sbmA0.07.118.9Spore maturation protein
spmB6.915.213.3Spore maturation protein
soj244.729.148.2Sporulation initiation inhibitor Soj
atoS5.34.110.0Sporulation kinase
kinA135.89.85.3Sporulation kinase
kinB283.550.743.5Sporulation kinase
kinE40.16.444.2Sporulation kinase
gerM8.824.057.5Sporulation protein
spo0B31.18.6199.6Sporulation protein
spo0M13.343.146.0Sporulation protein Spo0M
ypjB0.04.28.0Sporulation protein YpjB
ytaF0.036.87.5Sporulation protein YtaF
whiA137.423.532.1Sporulation regulator WhiA
yaaT143.78.165.0Stage 0 sporulation protein
spo0A679.5131.2132.2Stage 0 sporulation protein A
spo0F363.335.133.7Stage 0 sporulation protein F
spoIIB1.91.84.2Stage Ⅱ sporulation protein B
spoIID3.891.719.0Stage Ⅱ sporulation protein D
spoIIIAB0.02.34.8Stage Ⅲ sporulation protein AB
spoIIIAD0.023.228.3Stage Ⅲ sporulation protein AD
spoIIID0.00740.9111.4Stage Ⅲ sporulation protein D
spoIVA15.6428.7222.0Stage Ⅳ sporulation protein A
spoVAA0.015.32.6Stage Ⅴ sporulation protein AA
spoVD50.79.251.2Stage Ⅴ sporulation protein D
spoVE/ftsW75.622.2112.2Stage Ⅴ sporulation protein E
spoVFB5.93 281.5167.9Stage Ⅴ sporulation protein VFB
spoVID0.848.131.7Stage Ⅵ sporulation protein D
hcN/YlaJ3.7148.814.3YhcN/YlaJ family sporulation lipoprotein
), ArticleFig(id=1241084449132171446, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表5, caption=

芽胞形成基因转录水平

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
spoIIAA218.545.675.4Anti-sigma F factor antagonist
ftsK3.049.57.0Cell division protein FtsK
rsfA58.6345.789.9Prespore-specific transcriptional regulator rsfA
gerA2.420.412.7Spore germination protein GerA
gerD163.469.39.2Spore germination protein GerD
gerQ10.0645.3392.4Spore germination protein GerQ
sbmA0.07.118.9Spore maturation protein
spmB6.915.213.3Spore maturation protein
soj244.729.148.2Sporulation initiation inhibitor Soj
atoS5.34.110.0Sporulation kinase
kinA135.89.85.3Sporulation kinase
kinB283.550.743.5Sporulation kinase
kinE40.16.444.2Sporulation kinase
gerM8.824.057.5Sporulation protein
spo0B31.18.6199.6Sporulation protein
spo0M13.343.146.0Sporulation protein Spo0M
ypjB0.04.28.0Sporulation protein YpjB
ytaF0.036.87.5Sporulation protein YtaF
whiA137.423.532.1Sporulation regulator WhiA
yaaT143.78.165.0Stage 0 sporulation protein
spo0A679.5131.2132.2Stage 0 sporulation protein A
spo0F363.335.133.7Stage 0 sporulation protein F
spoIIB1.91.84.2Stage Ⅱ sporulation protein B
spoIID3.891.719.0Stage Ⅱ sporulation protein D
spoIIIAB0.02.34.8Stage Ⅲ sporulation protein AB
spoIIIAD0.023.228.3Stage Ⅲ sporulation protein AD
spoIIID0.00740.9111.4Stage Ⅲ sporulation protein D
spoIVA15.6428.7222.0Stage Ⅳ sporulation protein A
spoVAA0.015.32.6Stage Ⅴ sporulation protein AA
spoVD50.79.251.2Stage Ⅴ sporulation protein D
spoVE/ftsW75.622.2112.2Stage Ⅴ sporulation protein E
spoVFB5.93 281.5167.9Stage Ⅴ sporulation protein VFB
spoVID0.848.131.7Stage Ⅵ sporulation protein D
hcN/YlaJ3.7148.814.3YhcN/YlaJ family sporulation lipoprotein
), ArticleFig(id=1241084449220251834, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 6, caption=

Transcription ofcry1Ac and molecular chaperone

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
cry1Ac207.56 547.25 537.0Pesticidal crystal protein cry1Ac
hsp20213.163.0702.9Molecular chaperone small heat shock protein
hsp20B31.711 694.1366.6Molecular chaperone small heat shock protein
dnaK2 366.9403.5862.7Molecular chaperone DnaK
groEL11 932.43 768.12 919.2Molecular chaperone GroEL
copZ48.168.2170.2Copper chaperone CopZ
htpG28.73.217.1Chaperone protein HtpG
dnaJ264.0101.9126.2Molecular chaperone DnaJ
clpB104.440.047.7Protein disaggregation chaperone
), ArticleFig(id=1241084450696646844, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表6, caption=

cry1Ac和分子伴侣的转录

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
cry1Ac207.56 547.25 537.0Pesticidal crystal protein cry1Ac
hsp20213.163.0702.9Molecular chaperone small heat shock protein
hsp20B31.711 694.1366.6Molecular chaperone small heat shock protein
dnaK2 366.9403.5862.7Molecular chaperone DnaK
groEL11 932.43 768.12 919.2Molecular chaperone GroEL
copZ48.168.2170.2Copper chaperone CopZ
htpG28.73.217.1Chaperone protein HtpG
dnaJ264.0101.9126.2Molecular chaperone DnaJ
clpB104.440.047.7Protein disaggregation chaperone
), ArticleFig(id=1241084450826670272, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=EN, label=Table 7, caption=

Transcription of PHB and acetoin related genes

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
ccmA0.01.86.8Acetoin ABC transporter ATP-binding protein
acoR21.12.42.5Acetoin dehydrogenase
alsD4.05.475.3Alpha-acetolactate decarboxylase
acuB103.3112.742.7Acetoin utilization protein AcuB
acuA42.747.714.8Acetoin utilization protein AcuA
gi|4463906543.81.96.8Acetoin ABC transporter permease
acuC211.840.926.1Acetoin utilization protein AcuC
phbB230.411.046.9Acetoacetyl-CoA reductase
phaC598.680.5253.5Poly(R)-hydroxyalkanoic acid synthase
), ArticleFig(id=1241084450944110786, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1241045261619876161, language=CN, label=表7, caption=

PHB和羟基丁酮相关基因转录

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneFPKMDescription
T1T2T3
ccmA0.01.86.8Acetoin ABC transporter ATP-binding protein
acoR21.12.42.5Acetoin dehydrogenase
alsD4.05.475.3Alpha-acetolactate decarboxylase
acuB103.3112.742.7Acetoin utilization protein AcuB
acuA42.747.714.8Acetoin utilization protein AcuA
gi|4463906543.81.96.8Acetoin ABC transporter permease
acuC211.840.926.1Acetoin utilization protein AcuC
phbB230.411.046.9Acetoacetyl-CoA reductase
phaC598.680.5253.5Poly(R)-hydroxyalkanoic acid synthase
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苏云金杆菌Bt4.0718不同时期比较转录组揭示芽胞和杀虫伴胞晶体形成机制
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谢俊雁 1, 2 , 罗斯思 1 , 朱梓榕 1 , 陈文慧 1 , 周客轩 1 , 夏立秋 1 , 丁学知 1, *
微生物学报 | 研究报告 2024,64(1): 108-129
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微生物学报 | 研究报告 2024, 64(1): 108-129
苏云金杆菌Bt4.0718不同时期比较转录组揭示芽胞和杀虫伴胞晶体形成机制
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谢俊雁1, 2, 罗斯思1, 朱梓榕1, 陈文慧1, 周客轩1, 夏立秋1, 丁学知1, *
作者信息
  • 1 湖南师范大学生命科学学院 省部共建淡水鱼类发育生物学国家重点实验室 微生物分子生物学湖南省重点实验室, 湖南 长沙 410081
  • 2 中国科学院亚热带农业生态研究所 畜禽养殖污染控制与资源化技术国家工程实验室, 湖南 长沙 410125
Comparative transcriptomics ofBacillus thuringiensis Bt4.0718 reveals the mechanisms of sporulation and parasporal crystal formation
Junyan XIE1, 2, Sisi LUO1, Zirong ZHU1, Wenhui CHEN1, Kexuan ZHOU1, Liqiu XIA1, Xuezhi DING1, *
Affiliations
  • 1 Hunan Provincial Key Laboratory of Microbial Molecular Biology, State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal University, Changsha 410081, Hunan, China
  • 2 National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, Hunan, China
出版时间: 2024-01-04 doi: 10.13343/j.cnki.wsxb.20230213
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摘要
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【目的】苏云金芽胞杆菌(Bacillus thuringiensis, Bt)在形成芽胞的过程中产生大量杀虫晶体蛋白(insecticidal crystal proteins, ICPs)，是目前应用最广泛、最安全的微生物杀虫剂的主要菌株资源。本研究旨在比较Bt 3个重要时期的转录组，进一步探究芽胞和杀虫伴胞晶体的形成机制，为高效工程菌的构建奠定理论基础。【方法】选取高毒力Bt4.0718菌株营养生长中期(T1-10 h)、芽胞形成前期(T2-20 h)、芽胞形成后期(T3-32 h)进行比较转录组分析，对代表性差异基因进行实时荧光定量PCR (real-time fluorescence quantitative PCR, qRT-PCR)验证、特定功能基因的敲除和表型分析验证。【结果】差异表达基因数量分别为2 147个(T2/T1)、1 861个(T3/T1)、1 708个(T3/T2)。T1时期，培养基中营养相对丰富，主要为芽胞和杀虫伴胞晶体形成做准备。芽胞形成重要调控基因kinA/D、spo0A/F、sigE高水平转录对菌体的生长发育具有重要作用，Cry1Ac、碳源、能源贮藏物聚-羟基丁酸(poly-hydroxybutyric acid, PHB)和羟基丁酮(acetoin)也已开始转录。芽胞和ICPs的大量形成在T2和T3时期，相关基因的转录水平T2比T3时期高。T2对比T3时期，芽胞核/衣/皮质(spore core/coat/cortex)、芽胞萌发受体蛋白(germination protein)和芽胞形成的Ⅱ−Ⅵ阶段相关基因(spoⅡ−spoⅥ)在T2时才开始大量转录，为3个时期的最高水平；相应的糖类、氨基酸、脂质代谢，能量、核酸、多肽代谢、次级产物生成和环境适应系统等复杂网络均表现出差异；另外，作为营养信号刺激性生理过程，双组分信号转导系统(two-component signal transduction system, TCS)和ABC转运系统在芽胞形成和ICPs的转录表达过程中发挥重要作用，转录水平具有显著差异。【结论】随着芽胞和杀虫伴胞晶体的形成，营养成分逐渐匮乏，sigB、sigW和sigM的高效表达有助维持细胞壁的稳定和对环境变化的抗性；小热激蛋白Hsp20和Hsp20B作为分子伴侣蛋白对维持胞内稳态也十分重要，T2、T3时期高水平转录可能有助于芽胞形成和ICPs表达。

苏云金芽胞杆菌  /  比较转录组  /  芽胞  /  杀虫伴胞晶体

[Objective] Bacillus thuringiensis (Bt), characterized by the massive production of insecticidal crystal proteins (ICPs) during sporulation, serves as the main strain resource for the commonly used and safe microbial insecticides. To further explore the mechanisms of sporulation and parasporal crystal formation and lay a theoretical foundation for the construction of efficient strains, we compared the transcriptomes of Bt at three important stages.[Methods] The transcriptomes of the hypervirulent strain Bt4.0718 at the middle vegetative growth stage (T1-10 h), the early sporulation stage (T2-20 h), and the late sporulation stage (T3-32 h) were compared. The representative differentially expressed genes (DEGs) were verified by real-time fluorescence quantitative PCR (qRT-PCR), and the phenotypes of the mutant strains with the knockout of specific functional genes were examined.[Results] The number of DEGs was 2 147 (T2/T1), 1 861 (T3/T1), and 1 708 (T3/T2), respectively. At T1, the medium was rich in nutrients, which served the sporulation and parasporal crystal formation. The high transcription levels ofkinA/D,spo0A/F, andsigE regulating sporulation played a role in the growth and development of the cells. The transcription of Cry1Ac, poly-hydroxybutyric acid (PHB), and hydroxybutanone (acetoin) were started at this time. The substantial formation of ICPs and spores occurred at T2 and T3, and the transcript levels of the regulatory genes were higher at T2 than those at T3. The genes associated with spore core/coat/cortex, germination protein, andspoII–spoVI began to be transcribed in large amounts at T2, with the highest levels among the three stages. The corresponding complex networks of carbohydrate, amino acid, and lipid metabolism, energy, nucleic acid, and peptide metabolism, secondary metabolite production, and environmental adaptation showed differences. In addition, as the physiological processes stimulated by nutrient signals, the two-component signal transduction system (TCS) and ABC transport system played an essential role in the process of sporulation and ICP transcription and expression, and their transcription levels were significantly different.[Conclusion] With the production of ICPs and sporulation, nutrients are gradually consumed, and the high expression ofsigB,sigW, andsigM contributed to the stability of cell wall and the resistance to environmental changes. Meanwhile, the small heat shock proteins Hsp20 and Hsp20B, as molecular chaperones, were also important for maintaining intracellular homeostasis and may facilitate the sporulation and ICP production.

Bacillus thuringiensis  /  comparative transcriptomics  /  sporulation  /  insecticidal parasporal crystals
谢俊雁, 罗斯思, 朱梓榕, 陈文慧, 周客轩, 夏立秋, 丁学知. 苏云金杆菌Bt4.0718不同时期比较转录组揭示芽胞和杀虫伴胞晶体形成机制. 微生物学报, 2024 , 64 (1) : 108 -129 . DOI: 10.13343/j.cnki.wsxb.20230213
Junyan XIE, Sisi LUO, Zirong ZHU, Wenhui CHEN, Kexuan ZHOU, Liqiu XIA, Xuezhi DING. Comparative transcriptomics ofBacillus thuringiensis Bt4.0718 reveals the mechanisms of sporulation and parasporal crystal formation[J]. Acta Microbiologica Sinica, 2024 , 64 (1) : 108 -129 . DOI: 10.13343/j.cnki.wsxb.20230213
正文
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苏云金芽胞杆菌(Bacillus thuringiensis, Bt)是革兰氏阳性细菌，也是最安全的微生物农药菌剂之一，已在全球范围内害虫防治应用数十年[1]。高通量筛选的B4F11菌株中鉴定出一种新的杀虫蛋白Cry78Ba1，在稻飞虱的高效、安全防控方面具有巨大的应用潜力[2]。除了在农业害虫防治方面的应用外，Bt还能够促进植物生长[3]、生物修复重金属污染、生物合成金属纳米颗粒[1]、产生黑色素[4]，甚至杀死癌细胞[5]，所产的伴胞活性素对人类结肠癌细胞具有很好的杀伤活性，且没有溶血活性[6-7]。在能源应用方面，糖工业废水和食品工业废水产氢菌株鉴定中也发现有Bt菌株的存在[8]。
Bt的芽胞形成机制大都来自模式菌株枯草芽胞杆菌(Bacillus subtilis) 168的相关研究。目前，利用转录组学方法对Bt中杀虫伴胞晶体和芽胞形成机制的研究很少，2013年Wang等对Bt CT-43菌株芽胞形成的4个不同阶段进行转录组学和定量蛋白质组学的比较分析，较全面地绘制了芽胞形成调控网络，代谢方面主要包括氨基酸、碳源和能量的供应[9]。Bt4.0718与Bt CT-43相比，所含的内生质粒数量、杀虫毒力基因和基因组大小及杀虫晶体形成机制方面也可能存在一定的差异。因此，根据芽胞和伴胞晶体形成的时间调控特征，选取Bt4.0718的3个关键时期进行比较转录组分析，以期能够补充或完善芽胞和伴胞晶体形成机制，挖掘到一些功能基因，为进一步改良和构建工程菌奠定基础。
1 材料与方法
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1.1 材料
本实验室筛选的高毒力野生型Bt4.0718菌株，LB液体培养基(g/L)：酵母提取物(yeast extract) 5，氯化钠(NaCl) 10，胰蛋白胨(tryptone) 10；牛肉膏发酵培养基(g/L)：牛肉膏5，葡萄糖3，蛋白胨10，NaCl 2，K2HPO4 0.3，MnSO4·H2O 0.05，MgSO4·7H2O 0.3。培养条件：20 mL发酵培养基/250 mL摇瓶，30 ℃、120 r/min培养。
1.2 RNA提取和质量检测
采用TRIzol结合液氮研磨方法，按试剂盒操作说明提取总RNA [生工生物工程(上海)股份有限公司)]。经Agilent 2100 Bioanalyzer、Agilent RNA 6000 Nano Kit (安捷伦)等仪器检测RNA样品质量(深圳华大基因科技服务有限公司)。
1.3 转录组文库构建及测序
取1 μg质检合格的总RNA，按标准操作手册去除rRNA。合成cDNA，末端修复加“A”碱基，接头连接，3步处理均按照测序公司标准体系进行操作(深圳华大基因科技服务有限公司)。
1.4 参考基因组比对及新转录本预测
使用HISAT将过滤后的clean reads比对到参考基因组-模式菌株Bt-HD73，利用Rockhopper软件把所有样品的重构信息进行整合的转录本与参考注释信息进行比较，把IGR类型的转录本定义为新转录本，使用coding potential calculator (CPC)软件对每个新转录本进行蛋白编码能力预测，分为具有蛋白编码能力的转录本(coding)和不具有蛋白编码能力的转录本(non-coding)。
1.5 参考基因集比对及定量
用Bowtie2软件将clean reads比对到参考基因，使用RSEM计算每个基因的reads count，将reads count换算为每百万个映射读取的外显子模型每千碱基读取数(reads per kilobase of exon model per million mapped reads, FPKM)，即每1百万个映射上的reads中映射到外显子的每1 000个碱基上的reads个数，计算方法：1 000 (reads个数)/1 (百万)×n (K)=FPKM，FPKM的值反映出这个基因的表达水平。
1.6 差异表达基因筛选
使用DESeq2算法进行差异表达基因检测。DESeq2采用负二项分布模型，对估算的基因表达量进行差异显著性检验，并对统计学中的P value进行校正。当组间存在共有基因时，用Venn图分析对重叠情况进行展示。
1.7 生物信息学分析
主成分分析(principal component analysis, PCA)，用R软件中的ade4软件包将数据间大部分的方差降到相同的维度或坐标轴，实现对大数据整体差异的比较观察和简化。
时间序列分析，在不同时间阶段一些基因会有相似的表达模式，根据基因的表达量信息，可以聚类成与时间相关联的基因簇，表达模式一致的基因会被聚到同一个簇(cluster)，从而直观反应时间对基因表达的影响，有助于找到功能相似的基因；同时表达趋势一致的基因可能参与同一个生物过程。使用时间序列分析软件Mfuzz (v2.34.0)基于宽松聚类算法根据相似的表达谱将基因归为多个簇(深圳华大基因科技服务有限公司)。
通路(pathway)、基因本体(gene ontology, GO)富集分析，两者的条目显著性分析按照公式(1)计算。
式中N为所有基因中具有注释的基因数目；n为N中显著差异表达基因的数目；M为所有基因中注释为某特定条目(term)的基因数目；m为注释为某特定条目的显著差异表达基因数目。计算得到的P value通过校正之后，以P value≤0.05为标准，来定义显著差异表达基因中富集的term。
1.8 实时荧光定量PCR (real-time fluorescence quantitative PCR, qRT-PCR)验证
取1 μg总RNA用DNase Ⅰ消化残留的基因组DNA，按照逆转录试剂盒Revert AidTM First Strand cDNA Synthesis Kit (Thermo Fisher)操作说明将RNA反转录为cDNA。参照ABI公司的Power UPTM SYBRTM Green Master Mix手册，按20 μL体系添加引物、模板，进行qRT-PCR分析，以16S rRNA基因作为内参。采用2−ΔΔCt相对定量法分析不同基因mRNA表达水平变化。所用引物见表1。
1.9 三亲本接合转移及hsp20无痕敲除菌株的构建
利用Ⅰ-Sce Ⅰ介导的无痕敲除技术体系[10]构建敲除突变株。三亲本结合转移操作：(1) Bt 4.0718菌株、pRP1028-hsp20UD/DH5α、pSS1827/DH5α进行接合转移(1:1:1)，将敲除载体pRP1028-hsp20UD导入Bt 4.0718，经过第一次同源单交换pRP1028-hsp20UD整合到Bt 4.0718基因组上；(2) 同样用三亲本结合转移的方法在整合有pRP1028-hsp20UD的Bt 4.0718菌株中导入表达归巢内切酶Ⅰ-Sce Ⅰ的pSS4332质粒；(3) Ⅰ-Sce Ⅰ表达，识别并剪切同向重复序列之间的Ⅰ-Sce Ⅰ酶切位点，基因组断裂，断裂的DNA再次进行同源单交换，hsp20基因片段被敲除或者回复成野生型。
1.10 生长曲线测定和相差显微镜形态观察
活化的菌株(OD600=0.6)按1%的比例接种到发酵培养基，30 ℃、120 r/min培养。测量生长曲线至50 h，每组设3个生物学重复。每隔2 h取1次样，分光光度计测定发酵液OD600值(无菌发酵培养基作为空白对照)，时间为横坐标、OD600值为纵坐标绘制生长曲线。用100×相差显微镜观察。
1.11 扫描电子显微镜样品的制备及观察
发酵样品的10倍稀释液(菌体或伴胞晶体和芽胞混合物)无菌超纯水洗10−15次(9 000×g, 3 min)，4 ℃条件下用2.5%戊二醛溶液固定12 h。纯净水洗涤3次，样品分别用30%、50%、70%、80%、90%、95%和100%乙醇依次进行脱水2次，每次10 min。适量无水乙醇打匀，样品涂片，冷冻干燥后喷射镀金。扫描电子显微镜(Hitachi Su8010)成像，放大倍数5 000×−20 000×。
1.12 芽胞形成计数
Bt菌株发酵培养60 h (30 ℃)，OD600稀释至1.0。发酵液混匀后取1 mL细胞置65 ℃处理30 min；再梯度稀释(10×)，稀释的10−5、10−6、10−7样品取100 μL涂布在LB平板上，计算每毫升的菌落形成单位(colony forming units, CFU)，每组设置3个生物学重复。
1.13 ICP的提取与浓度测定
提取ICP，Bt菌株用GYS发酵培养20−24 h，细胞OD600稀释至1.0后收集20 mL培养物，8 000×g离心10 min，细胞沉淀用磷酸盐缓冲液(phosphate buffered solution, PBS)洗涤2次，加25 mL PBS重悬；冰上超声破碎(380 W, 3 s, 3 s, 10 min)，离心10 min (12 000×g, 4 ℃), 沉淀用1 mol/L NaCl和无菌水依次洗涤2次；5 mL含5% β-巯基乙醇的50 mmol/L Na2CO3-NaHCO3 (pH 10.0)溶液重悬沉淀，37 ℃孵育1 h溶解伴胞晶体蛋白再离心10 min (12 000×g, 4 ℃)，上清液经十二烷基硫酸钠-聚丙烯酰胺凝胶电泳(sodium dodecyl sulfate polyacrylamide gel electrophoresis, SDS-PAGE)可视化分析，Bradford法测量ICPs含量。
2 结果与分析
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2.1 Bt4.0718三个重要时期相差显微镜观察
选取不同发酵时间(T1-10 h，营养生长期；T2-20 h，芽胞形成前期；T3-32 h，芽胞形成后期)相差显微镜观察。T1时期，菌体呈短杆状，正常生长，胞内无明显折光性强的物质，无芽胞迹象；T2时期，胞内芽胞形成，芽胞附近有可见的内含物，少数发育快的个体芽胞发育完全，芽胞旁边能够观察到菱形晶体；T3时期，胞内芽胞基本发育完全，且都伴有菱形或不规则晶体(图1)。
2.2 转录组测序
提取3个时期菌体RNA (每个时期3个生物学重复)，质量均达到测序要求。测序结果与参考基因组的平均比对率为69.52%，完美匹配的平均比率为55.4%，平均的唯一匹配比率为68.5%，数据匹配结果良好。大部分基因的reads覆盖率能达到90%以上。共鉴定到32个新转录本，均为非编码sRNA。PCA二维图(图2)上，不同时期样品的位置分散、距离较远，生物学重复则比较聚集，表明重复性良好，组别间差异较大。数据差异性最大和次大2个主成分因子(第一主成分PC1和第二主成分PC2)的百分比(即对总体方差的贡献率)分别为55.6%和42.6%，PC1和PC2可以解释总体方差(反应样本离散程度)的98.2%，通过数据的降维处理，仅丢失了约1.8%的离散关系信息。
2.3 显著差异基因统计分析
T1时期共检测到3 785个转录本，T2和T3时期分别鉴定3 549个和3 822个。另外，T1-T2-T3共同基因为2 783个；两两相互共有的转录本为211、353、471个；3个时期特有的转录基因数分别是320、202、215个(图3A)。T2相对T1时期显著差异基因共有2 147个，上调基因数为1 250，下调基因数为897；T3相对T1时期共筛选到1 861个显著差异基因，其中上调992个，下调869个；T3对比T2时期，显著差异基因共有1 708个，上调838个，下调870个(图3B)。
2.4 芽胞结构和组分相关基因
Bt芽胞呈椭圆或圆形，抗逆性强，细胞壁很厚，含水量很低，主要的结构包括芽胞外壁(exosporium)、芽胞衣(spore coat)、皮层(cortex)、内核(core)，吡啶二羧酸钙盐(pyridine dicarboxylic acid calcium salt, DPA)、酸溶性芽胞蛋白(acid-soluble spore protein)为重要组分。3个时期转录组共检测到29个相关基因(表2)，其中酸溶性芽胞蛋白合成基因10个，芽胞衣形成相关基因15个，DPA合成基因3个(dapA/B/D)，而皮层合成基因仅鉴定到1个(yabQ)。以上基因均在T2和T3时期高效转录，且T3时期的转录水平相对T2时期明显降低。
除上述相关基因外，还鉴定到大量芽胞肽聚糖(细胞壁)合成相关基因，主要涉及丙氨酸酰胺酶(alanine amidase)、细胞壁水解酶(hydrolase)、丙氨酸羧肽酶(carboxypeptidase)、细胞壁结合蛋白(penicillin-binding protein)，共32个(代表性基因如表3所示)，其中肽聚糖识别(recognition)和翻转(turnover)蛋白基因各1个。2个细胞壁水解酶的转录水平T2时期最高，而大多数细胞壁结合蛋白在T2时期转录水平相对最低。乙酰胞壁酰-丙氨酸酰胺酶在T3时期相对转录水平最高，cwlA在3个时期的转录无明显变化，cwlD主要在T2时期高效转录，而cwlO主要在T1和T3时期转录。
2.5 Sigma转录调控基因
芽胞和ICPs的形成过程中主要受到sigma转录因子的时序调控。共鉴定到16个sigma因子及其相关基因(表4)，主要是sigma70家族基因，包括rpoD/E、sig54和sigE-H。sigK相关基因有2个，bofA和bofC，主要对sigK转录水平进行调控。另外还检测到低转录水平的sigW、sigX和sigM负效应子。sigE、sigG和bofC主要在T2和T3时期高效转录，sig54和sigF在3个时期都能高效转录，而sigH在T1时期的转录效率最高。
2.6 转录组中芽胞形成基因
芽胞形成相关基因共87个，包括芽胞形成激酶、芽胞萌发受体蛋白，从起始到第Ⅵ阶段的芽胞形成蛋白基因(spo0−spoVI)，芽胞发育成熟基因(sbmA、spmB)，以及其他芽胞形成调控基因。其中spo0A/F和芽胞形成激酶(kinA/B/E)早在T1时期高效转录。其他大部分基因在T2和T3时期的转录水平明显要比T1时期高，趋势与表型相符。spoIIAA、spoIISA/B、spoVG比较特殊，在T1时期转录水平最高(表5)。
2.7 Cry1Ac和分子伴侣蛋白转录变化
对分子伴侣蛋白进行检索，共鉴定到8个功能基因(表6)，在3个时期都能进行有效转录。hsp20B与cry1Ac的转录变化趋势基本一致，hsp20转录水平在T2时期最低，T3时期最高；dnaK、dnaJ、groEL、clpB和htpG 3个时期中在T1时期表现出最高转录；只有copZ表现出不断递增的趋势。
2.8 碳源、能源储藏物PHB和羟基丁酮的转录
phbB和phaC与PHB合成相关，均在T1时期高效转录，在T2时期显著下调，到T3时期转录水平又逐渐回升。羟基丁酮合成相关基因有7个(表7)，其中acetoin利用蛋白基因acuA/B/C在T1−T3均有效转录。
2.9 差异基因的qRT-PCR验证
选取一些上下调基因和几个重要代表性基因进行转录水平的验证。以T1时期的转录水平作参照设为1。杀虫晶体蛋白Cry1Ac、Cry2Aa，芽胞和ICPs形成转录调控因子sigmaK，芽胞皮层形成功能蛋白CwlD，它们均在T2、T3时期显著上调，而且T2时期倍数差异基本在150倍以上，比T3时期的更高(图4)。整体的qRT-PCR结果和转录组的差异变化趋势相一致，与菌株的表型和已有的相关研究相符。
其他功能基因(图5A)，如小热激蛋白基因hsp20，氨基酸合成相关基因leuB、glnA、lysA，芽胞起始相关基因spo0A、phoR，转录水平的验证结果与转录组的变化趋势相一致。此外，pyrG、odhB、pgk和hslV等代谢相关基因的转录水平变化(图5B)也基本与qRT-PCR结果相符，在T2、T3时期显著下调。
2.10 差异基因的生物信息学分析
T2/T1、T3/T1、T3/T2三组差异基因所富集的通路无差异，都包含了细菌的生长，复制、转录和翻译，环境信息相关的信号转导和膜转运；代谢最显著的包括糖类、氨基酸、脂质和能量代谢，核酸、多肽代谢和次级产物生成代谢，菌体的免疫系统和环境适应系统也有所涉及。对3组差异基因再次进行Venn分区，去除一些重复性的干扰，对每组特异性的显著差异基因进行分筛，结合每个时期的特点进一步分析。根据3组显著差异基因的韦恩图，进行编号Ⅰ−Ⅶ (图6)，T2/T1组的特异性差异基因为218个(Ⅰ)，T3/T1组特异性差异基因有243个(Ⅱ)，T3/T2组特有的差异基因数为163个(Ⅲ)。3组共同含有的差异基因有576个(Ⅶ)，而3组间两两共同包含的差异基因数分别为663 (Ⅳ)、346 (Ⅴ)、588 (Ⅵ)。
2.10.1 I–VII号区域差异基因集的KEGG分析
在菌株库中选择枯草芽胞杆菌模式菌株Bacillus subtilis 168为模型，对Ⅰ−Ⅶ区域进行KEGG通路分析。Ⅰ号区域富集到的双组分系统和ABC转运子最为显著，其次磷酸转移酶系统、乙醛酸和二羧酸代谢较为明显，非核糖体肽模块(non-ribosomal peptide structures)也在此区域被富集到；Ⅱ号区，双组分系统、氨基酸合成(其中支链氨基酸的合成被单独富集)富集程度最高，而且非核糖体肽模块、淀粉和蔗糖代谢、泛酸和辅酶A (coenzyme A, CoA)合成途径也被富集(图7)。
在其他区域中，Ⅲ号区未发现值得被关注的通路，因此未展示。Ⅳ号区除去映射到132个基因的最显著的代谢途径(metabolic pathways)，脂肪酸合成与代谢、嘧啶代谢(pyrimidine metabolism)、氧化磷酸化、丙氨酸(Ala)、天冬氨酸(Asp)和谷氨酸(Glu)代谢都被相对均匀涉及。Ⅴ号区主要富集到甘油磷脂代谢(glycerophospholipid metabolism)赖氨酸降解(lysine degradation)、支链氨基酸降解、嘌呤代谢(purine metabolism)和核糖体代谢，而最后2个途径比较突出，分别映射到21个和25个基因(图8)。
针对Ⅵ和Ⅶ号区的KEGG分析(图9)，Ⅵ号区差异基因映射最多的是次级代谢物合成，其次是氨基酸合成，另外与细胞壁合成相关的d型丙氨酸(d-alanine)代谢、肽聚糖合成通路富集9个差异基因；Ⅶ号区，124个基因映射到代谢途径，氨基酸合成映射到差异基因29个，嘧啶代谢映射到15个，赖氨酸生成映射到6个，精氨酸合成映射到7个，硫胺素合成和硫传递系统分别映射到8个和6个。
2.10.2 时间序列聚类
芽胞和杀虫伴胞晶体的形成与培养时间有关，根据所选3个时期，时间表达模式共得到9类基因簇(cluster 1−9，图10)。qRT-PCR验证和转录测序结果表明，杀虫晶体蛋白的表达模式归类到cluster 2，同时，对各类基因簇的分析发现，在cluster 7集中了大量与芽胞和ICPs相关的功能基因。Cluster 2和cluster 7所包含的基因个数分别为732和866。Cluster 2中主要包含了基础代谢、碳源和能源代谢，以及部分的氨基酸修饰(图11)，其中，发挥催化和氧化还原活性的功能基因占主导地位，分别聚集到273个和83个基因，而第三大类富集在物质转运，主要是糖类和特异性底物的转膜、转运。
Cluster 7基因簇富集最显著的通路是双组分系统、ABC转运系统(橙色条目)，加上非核糖体肽，这3类条目与之前显著差异基因韦恩图中Ⅰ和Ⅱ号区的分析结果相重合。除此以外，甘油磷脂代谢和细菌趋化性通路也被匹配到，而这两者在之前并未显著富集(图12)。
2.11hsp20基因的功能研究
根据以上3个时期的转录组比较分析，对芽胞和ICPs形成时期高效转录的小热激蛋白基因hsp20的功能研究。利用Ⅰ-Sec Ⅰ无痕敲除体系构建Bt4-Δhsp20突变株(图13)，相比原始菌株Bt4.0718，敲除菌株的生长稳定期缩短了大约2 h，生长量略微减少，芽胞形成量约为原始菌的10%，ICP产量为原始菌的1/2 (图14，图15)，表明小热激蛋白基因hsp20对芽胞和ICPs的形成具有显著的影响。
3 讨论
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3.1 Bt芽胞形成不同时期转录特征
在T1时期，Bt主要是自身的生长发育，尽管芽胞形成起始激活的各个重要基因都已开始高水平转录，为芽胞形成的起始做好充足准备，在后续营养进一步匮乏时，芽胞形成的代谢网络会被陆续激活。与表型相符，WhiA主要影响细胞分裂[11]，在T1时高水平转录。Anti-sigma F因子spoIIAA，soj芽胞形成起始抑制子，芽胞形成激酶基因kinA/B/E，芽胞形成早期重要调控基因spo0A/F、yaaT转录水平T1最高。Soj作为染色质分配蛋白，控制着DNA的复制，细胞的分裂，在T1时期高效转录有利菌体正常的生长、发育和增殖[12-13]，Soj也可通过抑制磷酸化Spo0A激活的启动子转录而负调控芽胞的形成[14]。kinA/B/E在对数生长阶段调控spo0A和spo0F的磷酸化，同时在生长稳定期早期转录表达[15]。yaaT在芽胞起始的磷酸化信号转导和菌体的生长发育都具有重要作用[16]。另外，前芽胞特异转录调控基因rsfA在T1时期已开始进行有效的转录，芽胞萌发受体蛋白基因gerD、gerIA和gerQ与rsfA转录情况相同，为芽胞形成做好准备。
T2时期大量形成芽胞和ICPs，从芽胞形成的起始到发育成熟，相关基因均在此阶段进行高效转录。到T3时期，芽胞形成相关基因大都保持一定转录水平，但相对T2时期有不同程度的降低，直到芽胞发育成熟，杀虫伴胞晶体已大量成型。T3时期，菌体处于稳定中后期，培养基中的营养成分相对T2时期更为匮乏，因此芽胞形成相关基因的转录水平也会随之下调，但对芽胞形成起关键调控作用的spoA/F、kinA/B的转录水平与T2时期无显著变化，这对芽胞和ICPs形成提供了重要保证。
代谢层面，芽胞和ICPs的形成得益于早期能源的储备和重要代谢通路的稳定协同。聚-3-羟基丁酸(PHB)和羟基丁酮的合成主要发生在生长对数期，T1时期PHB合成相关的phaC和phbB转录水平最高，T2和T3时期都相应下调，T2时期最低。与羟基丁酮合成相关的acoR同样在T1时的转录最高(alsD3个时期无变化)，作为乙酰辅酶A的重要来源，它的利用可能在T1时就开始，且主要消耗在T1和T2时期，因为羟基丁酮利用操纵子acu (acuA/B/C)在T1和T2时期高转录，在T3时期显著下调。T2和T3时期相比T1共有的差异代谢途径包括脂肪酸代谢与合成、氧化磷酸化、2-氧代羧酸代谢、嘧啶代谢甘油磷脂代谢氨基酸(丙氨酸、天冬氨酸、谷氨酸、赖氨酸、精氨酸)代谢硫胺素代谢和氨基酸合成。除上述的差异代谢途径，时间序列分析中的cluste 2与杀虫晶体蛋白(Cry1Ac)的转录趋势相似；cluster 7的聚类结果是在T3时期上调的基因集，其中的一些上调基因很有可能有利杀虫晶体蛋白的表达。Cluster 2中的基因主要与催化和转运相关，其中较为突出的是物质的氧化还原，糖或其他底物的转膜、转运。与cluster 2不同，cluster 7以甘油磷脂代谢，双组分系统，ABC转运体为主，在后期作用显著，PhoP-PhoR双组分系统，主要介导磷酸盐缺乏反应，引发芽胞形成所需的Spo0蛋白的磷酸转移，且枯草芽胞杆菌中的Pho调节子受Res、Pho和Spo信号转导系统整体作用的调控[17]。LiaRS双组分系统在芽胞杆菌中主要维持细胞膜的完整性，对胞膜的扰动有所反应[18]，在T2时期上调，表明此时细胞膜上的活动增强。LytST能够调控丙酮酸的利用，细胞外丙酮酸充当LytST双组分系统的信号分子，进而诱导后续PftAB转运蛋白的表达，当丙酮酸大量流入时，LytST活性被大大地抑制[19]。T2与T1时期相比，大部分的ABC转运子ATP结合蛋白和通透酶基因的转录水平显著上调；葡萄糖转运子亚基、甲硫氨酸(Met)支链氨基酸、谷氨酰胺(glutamine)、半胱氨酸(cysteine)、甘氨酸(glycine)和甘油-3-磷酸(glycerol-3-phosphate)相关的ABC转运子转录上调，均有利于ICP的合成。而大部分肽段(peptide)和铁离子ABC转运子转录水平下调，其原因值得进一步研究。
3.2 芽胞和ICPs形成转录调控因子
转录调控因子sigma E/F/G/H/K与芽胞和ICPs形成的关系已研究和报道，各因子(表4)的转录趋势与已知研究结果相一致。其他调控基因如表4中bofA，仅在T1时低水平转录，在T2和T3时期无转录，而bofC在T1时低转录，在T2和T3时水平分别提高29倍和16倍，正好增强SigK的转化，将有利于芽胞和ICPs的形成。芽胞杆菌自身生长和应激反应相关调控因子SigB属一般性应激转录因子，与生物膜形成相关，营养有限时触发扩散至关重要，可提高对环境的适应性[20]。SigW在细胞膜上表达，正常情况下与抗-SigW因子紧密结合，当受到不同应激条件时，SigW解离出来激活其调控因子的转录[21]，应对环境变化；SigM负责调节细胞壁合成相关基因，在压力条件下维持细胞壁的稳态起关键作用[22]；SigX和SigM同属胞质外功能(extracytoplasmic function, ECF)的sigma因子，在对数生长期和早期稳定生长期与下游基因ypuN共转录，能够增强高温、高盐的耐受性，同时能够改变细胞表面特性[23-24]。而Sig54主要调节对氮源和碳源的利用，调控一些代谢通路[25]，例如γ-氨基丁酸(γ-aminobutyric acid, GABA)和羟基丁酮(acetoin)的代谢，aco操纵子的转录由羟基丁酮诱导，受Sig54控制，由AcoR正向调控[26]。以上的调控因子可以很好地维持菌体的正常生长，应对环境条件的变化，对芽胞和ICPs的形成均有很好的辅助作用。
3.3 Bt中分子伴侣蛋白
常见分子伴侣蛋白ClpB、DnaK、DnaJ和GroEL见表6，在T1−T3时期始终能良好地转录表达，辅助蛋白的折叠，解聚变性或未折叠的蛋白，但在T1时期水平最高，可能此时菌体的新陈代谢最活跃。CopZ作为铜伴侣蛋白与p型ATP酶转运蛋白CopA共同构成枯草芽胞杆菌中的铜解毒系统，维持胞内的铜稳态，还参与了重金属银离子和镉离子的解毒，解毒能力大小与它们之间的亲和力有关，Ag(+)的结合亲和力与Cu(+)非常相似，而Cd(2+)的结合明显较弱[27-28]。copZ的T1−T3转录水平呈递增趋势(FPKM值从48上升至170)，可能对胞内物质运输和稳态具有重要作用。根据比较转录组的研究结果，鉴定到的2个Hsp20家族基因，其中hsp20B转录水平变化与cry1Ac的相似，而hsp20却在T3时期的转录水平最高，研究结果表明hsp20对Bt芽胞和伴胞晶体的形成发挥重要作用[29]。
综上所述，Bt4.0718杀虫晶体蛋白在对数生长中后期已开始转录表达，与芽胞形成不同步；芽胞形成的起始在营养逐渐匮乏时被诱导，但在早期对数中后期会被抑制。SigB/M/W/X和分子伴侣蛋白的表达上调能够很好地维持细胞壁的稳定和胞内稳态，为芽胞和ICPs的形成提供保障。芽胞和ICPs形成依赖基础代谢网络的协同，包括脂肪酸代谢、氧化磷酸化、嘧啶代谢、甘油磷脂代谢和氨基酸代谢等。参与底物特异性运输的ABC转运子表达上调，例如葡萄糖、支链氨基酸、半胱氨酸、甘油磷酸和磷酸盐等ABC转运子，能够促进芽胞和ICPs的形成。本研究对揭示Bt芽胞和ICPs形成机制具有一定科学指导意义，为挖掘更多相关功能基因，从调控、菌体代谢和稳态等层面进行修饰改造，构建高毒力、高效表达杀虫晶体蛋白Bt工程菌株提供理论依据。
基金
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  • 国家重点研发计划(2017YFD0201201)
  • 国家自然科学基金(31370116)
文献
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2024年第64卷第1期
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doi: 10.13343/j.cnki.wsxb.20230213
  • 接收时间：2023-03-30
  • 首发时间：2026-03-18
  • 出版时间：2024-01-04
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  • 收稿日期：2023-03-30
  • 录用日期：2023-09-27
基金
National Key Research and Development Program of China(2017YFD0201201)
国家重点研发计划(2017YFD0201201)
National Natural Science Foundation of China(31370116)
国家自然科学基金(31370116)
作者信息
    1 湖南师范大学生命科学学院 省部共建淡水鱼类发育生物学国家重点实验室 微生物分子生物学湖南省重点实验室, 湖南 长沙 410081
    2 中国科学院亚热带农业生态研究所 畜禽养殖污染控制与资源化技术国家工程实验室, 湖南 长沙 410125

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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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