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Article(id=1242175002213188097, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1242175008705966230, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20240439, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1721232000000, receivedDateStr=2024-07-18, revisedDate=null, revisedDateStr=null, acceptedDate=1730390400000, acceptedDateStr=2024-11-01, onlineDate=1774087199023, onlineDateStr=2026-03-21, pubDate=1735920000000, pubDateStr=2025-01-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1774087199023, onlineIssueDateStr=2026-03-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1774087199023, creator=13701087609, updateTime=1774087199023, updator=13701087609, issue=Issue{id=1242175008705966230, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='1', pageStart='1', pageEnd='415', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1774087200568, creator=13701087609, updateTime=1774087310368, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1242175469299270453, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1242175008705966230, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1242175469299270454, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1242175008705966230, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=29, endPage=37, ext={EN=ArticleExt(id=1242175002750059013, articleId=1242175002213188097, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Research progress in tigecycline resistance genes tet(X) in Acinetobacter spp., columnId=1239895164987175635, journalTitle=Acta Microbiologica Sinica, columnName=Reviews, runingTitle=null, highlight=null, articleAbstract=

Acinetobacter spp. are the common opportunistic pathogens worldwide and pose a threat to the health of humans and animals. As the resistance rate to carbapenems aggravates, tigecycline has become one of the last lines for the treatment of multidrug-resistant Acinetobacter spp. infection. The rapid dissemination of tigecycline resistance genes tet(X3), tet(X4), tet(X5), tet(X6), and other variants in recent years has seriously affected the clinical application of new tetracycline antibiotics such as tigecycline, eravacycline, and omadacycline, whereas there is a lack of review on the tet(X) genes in Acinetobacter spp. This article comprehensively expounds the mechanisms of action, epidemiological characteristics, transmission risks, and inhibitors of tet(X) genes in Acinetobacter spp. and evaluates the diversity of their variants, bacterial hosts, geographical distribution, and sampling sources, aiming to provide a theoretical basis for the prevention and control of tet(X)-positive Acinetobacter spp.

, correspAuthors=Chong CHEN, authorNote=null, correspAuthorsNote=
*CHEN Chong, E-mail:
, copyrightStatement=Copyright ©2025 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=Chong CHEN, Yilin LÜ, Taotao WU, Jing LIU), CN=ArticleExt(id=1242175004209676835, articleId=1242175002213188097, tenantId=1146029695717560320, journalId=1192105938417971205, language=CN, title=不动杆菌属细菌中替加环素耐药基因tet(X)的研究进展, columnId=1192149543882997826, journalTitle=微生物学报, columnName=综述, runingTitle=null, highlight=null, articleAbstract=

不动杆菌属细菌是全球常见的条件致病菌，给人类和动物健康造成了巨大威胁。随着对碳青霉烯类抗生素耐药率的不断升高，替加环素成为治疗多重耐药不动杆菌感染的最后防线之一。近年来，替加环素耐药基因tet(X3)、tet(X4)、tet(X5)和tet(X6)等变异体的快速传播严重影响替加环素、依拉环素和奥马环素等新型四环素类抗生素的临床应用，但对不动杆菌属细菌中的tet(X)基因缺乏综述。本文通过对不动杆菌属细菌中tet(X)基因的作用机制、流行特征、传播风险和抑制剂的全面分析，进一步评估其变异体、细菌宿主、地理分布和样品来源多样性，同时为tet(X)阳性不动杆菌属病原菌的防控提供理论依据。

, correspAuthors=陈冲, authorNote=null, correspAuthorsNote=null, copyrightStatement=版权所有©《微生物学报》编辑部2025, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=3vfY7YQx/FnEu61ylDbQvg==, magXml=iorpuyEhI67hRb7GTin8gA==, pdfUrl=null, pdf=e9ZbvgHG1NcrV7dMA5evww==, pdfFileSize=405732, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=gZVy+Iqb0UiryA+fJsLmoQ==, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=陈冲, 吕一林, 吴涛涛, 刘静)}, authors=[Author(id=1243299999665205642, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, orderNo=0, firstName=null, middleName=null, lastName=null, nameCn=null, orcid=http://orcid.org/0000-0002-0161-6574, stid=null, country=null, authorPic=null, dead=0, email=chen_chong@yzu.edu.cn, emailSecond=null, emailThird=null, correspondingAuthor=1, authorType=1, ext={EN=AuthorExt(id=1243299999828783504, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, authorId=1243299999665205642, language=EN, stringName=Chong CHEN, firstName=Chong, middleName=null, lastName=CHEN, prefix=null, suffix=null, authorComment=null, nameInitials=null, affiliation=null, department=null, xref=1, 2, *, address=1 Institutes of Agricultural Science and Technology Development (Joint International Research Laboratory of Agriculture and Agri-product Safety), Yangzhou University, Yangzhou 225009, Jiangsu, China
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A novel inhibitor of monooxygenase reversed the activity of tetracyclines against tet(X3)/tet(X4)-positive bacteria[J]. eBioMedicine, 2022, 78:103943., articleTitle=A novel inhibitor of monooxygenase reversed the activity of tetracyclines against tet(X3)/tet(X4)-positive bacteria, refAbstract=null), Reference(id=1243300009999971241, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, doi=10.1038/nchembio.2376, pmid=null, pmcid=null, year=2017, volume=13, issue=7, pageStart=730, pageEnd=736, url=null, language=null, rfNumber=[33], rfOrder=34, authorNames=null, journalName=Nature Chemical Biology, refType=null, unstructuredReference=PARK J, GASPARRINI AJ, RECK MR, SYMISTER CT, ELLIOTT JL, VOGEL JP, WENCEWICZ TA, DANTAS G, TOLIA NH. Plasticity, dynamics, and inhibition of emerging tetracycline resistance enzymes[J]. Nature Chemical Biology, 2017, 13 (7):730-736., articleTitle=Plasticity, dynamics, and inhibition of emerging tetracycline resistance enzymes, refAbstract=null), Reference(id=1243300010134188981, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, doi=10.1021/acsinfecdis.8b00349, pmid=null, pmcid=null, year=2019, volume=5, issue=4, pageStart=618, pageEnd=633, url=null, language=null, rfNumber=[34], rfOrder=35, authorNames=null, journalName=ACS Infectious Diseases, refType=null, unstructuredReference=MARKLEY JL, FANG LT, GASPARRINI AJ, SYMISTER CT, KUMAR H, TOLIA NH, DANTAS G, WENCEWICZ TA. Semisynthetic analogues of anhydrotetracycline as inhibitors of tetracycline destructase enzymes[J]. ACS Infectious Diseases, 2019, 5 (4):618-633., articleTitle=Semisynthetic analogues of anhydrotetracycline as inhibitors of tetracycline destructase enzymes, refAbstract=null), Reference(id=1243300010289378237, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, doi=10.1038/s42003-023-04792-4, pmid=null, pmcid=null, year=2023, volume=6, issue=1, pageStart=423, pageEnd=null, url=null, language=null, rfNumber=[35], rfOrder=36, authorNames=null, journalName=Communications Biology, refType=null, unstructuredReference=KUMAR H, WILLIFORD EE, BLAKE KS, VIRGIN-DOWNEY B, DANTAS G, WENCEWICZ TA, TOLIA NH. Structure of anhydrotetracycline-bound Tet(X6) reveals the mechanism for inhibition of type 1 tetracycline destructases[J]. Communications Biology, 2023, 6 (1):423., articleTitle=Structure of anhydrotetracycline-bound Tet(X6) reveals the mechanism for inhibition of type 1 tetracycline destructases, refAbstract=null)], funds=[Fund(id=1243300004056642121, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=32402890, language=EN, fundingSource=National Natural Science Foundation of China(32402890), fundOrder=null, country=null), Fund(id=1243300004127945295, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=32402890, language=CN, fundingSource=国家自然科学基金(32402890), fundOrder=null, country=null), Fund(id=1243300004253774422, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=BK20210803, language=EN, fundingSource=Natural Science Foundation of Jiangsu Province(BK20210803), fundOrder=null, country=null), Fund(id=1243300004325077596, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=BK20210803, language=CN, fundingSource=江苏省自然科学基金(BK20210803), fundOrder=null, country=null), Fund(id=1243300004509626984, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=2023M732993, language=EN, fundingSource=China Postdoctoral Science Foundation(2023M732993), fundOrder=null, country=null), Fund(id=1243300004631261815, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, awardId=2023M732993, language=CN, fundingSource=中国博士后科学基金(2023M732993), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1243299999430324609, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, xref=null, ext=[AuthorCompanyExt(id=1243299999442907522, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, companyId=1243299999430324609, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1 Institutes of Agricultural Science and Technology Development (Joint International Research Laboratory of Agriculture and Agri-product Safety), Yangzhou University, Yangzhou 225009, Jiangsu, China), AuthorCompanyExt(id=1243299999451296131, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, companyId=1243299999430324609, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1 扬州大学 农业科技发展研究院(农业与农产品安全国际联合实验室), 江苏 扬州 225009)]), AuthorCompany(id=1243299999551959429, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, xref=2, ext=[AuthorCompanyExt(id=1243299999560348038, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, companyId=1243299999551959429, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2 College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, Jiangsu, China), AuthorCompanyExt(id=1243299999568736647, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, companyId=1243299999551959429, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2 扬州大学 生物科学与技术学院, 江苏 扬州 225009)])], figs=[ArticleFig(id=1243300003595268646, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, language=EN, label=Table 1, caption=

Strains of Acinetobacter spp. carrying tet(X) variants and their sources

, figureFileSmall=null, figureFileBig=null, tableContent=
tet(X) variantsBacterial speciesLocationSampling sourcesReferences
/: Duplicate naming of the same tet(X) variant.
tet(X2)A. pittiiChina: ZhejiangHuman[18]
tet(X3)A. baumannii, A. johnsonii, A. piscicola, A. towneri, A. indicus, A. lwoffii, A. schindleri, A. gandensis, A. nosocomialis, A. pittii, A. variabilisChina: Jiangsu, Shandong, Guangdong, Guangxi, Hainan, Fujian, Jiangxi, Hunan, Zhejiang, Shanghai; Ivory Coast; ColombiaCow, pig, chicken, human, soil, sewage, dust, vegetable[9-10, 19-21]
tet(X3.3), tet(X3.4), tet(X3.5), tet(X3.6)A. variabilisChina: GuangxiPig[20]
tet(X3.7), tet(X3.8), tet(X3.9)A. schindleriChina: GuangxiChicken[20]
tet(X4)A. baumannii, A. indicus, A. towneriChina: Qinghai, Jilin, HenanHuman, migratory bird, pig[9-10, 22]
tet(X5)A. baumanniiChina: Hebei, GuangdongHuman, duck, chicken[6, 23]
tet(X5.4)A. indicusChina: GuangxiPig[19]
tet(X6)/tet(X5.2)A. baumannii, A. indicus, A. variabilis, A. towneri, A. johnsonii, A. lwoffii, A. schindleriChina: Jiangsu, Shanghai, Zhejiang, Jiangxi, Hunan, Fujian, Guangdong, Hainan, Taiwan, Guangxi, QinghaiChicken, human, pig, soil, sewage, dust, vegetable, duck, migratory bird[6, 10, 19, 24-26]
tet(X6) variant/tet(X5.3)A. baumannii, A. piscicolaChina: Guangdong, ZhejiangChicken, pig, soil[10, 24]
tet(X15)A. variabilisChina: JiangsuChicken[27]
), ArticleFig(id=1243300003763040815, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1242175002213188097, language=CN, label=表1, caption=

携带tet(X)变异体的不动杆菌属菌株及来源

, figureFileSmall=null, figureFileBig=null, tableContent=
tet(X) variantsBacterial speciesLocationSampling sourcesReferences
/: Duplicate naming of the same tet(X) variant.
tet(X2)A. pittiiChina: ZhejiangHuman[18]
tet(X3)A. baumannii, A. johnsonii, A. piscicola, A. towneri, A. indicus, A. lwoffii, A. schindleri, A. gandensis, A. nosocomialis, A. pittii, A. variabilisChina: Jiangsu, Shandong, Guangdong, Guangxi, Hainan, Fujian, Jiangxi, Hunan, Zhejiang, Shanghai; Ivory Coast; ColombiaCow, pig, chicken, human, soil, sewage, dust, vegetable[9-10, 19-21]
tet(X3.3), tet(X3.4), tet(X3.5), tet(X3.6)A. variabilisChina: GuangxiPig[20]
tet(X3.7), tet(X3.8), tet(X3.9)A. schindleriChina: GuangxiChicken[20]
tet(X4)A. baumannii, A. indicus, A. towneriChina: Qinghai, Jilin, HenanHuman, migratory bird, pig[9-10, 22]
tet(X5)A. baumanniiChina: Hebei, GuangdongHuman, duck, chicken[6, 23]
tet(X5.4)A. indicusChina: GuangxiPig[19]
tet(X6)/tet(X5.2)A. baumannii, A. indicus, A. variabilis, A. towneri, A. johnsonii, A. lwoffii, A. schindleriChina: Jiangsu, Shanghai, Zhejiang, Jiangxi, Hunan, Fujian, Guangdong, Hainan, Taiwan, Guangxi, QinghaiChicken, human, pig, soil, sewage, dust, vegetable, duck, migratory bird[6, 10, 19, 24-26]
tet(X6) variant/tet(X5.3)A. baumannii, A. piscicolaChina: Guangdong, ZhejiangChicken, pig, soil[10, 24]
tet(X15)A. variabilisChina: JiangsuChicken[27]
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不动杆菌属细菌中替加环素耐药基因tet(X)的研究进展
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陈冲 1, 2, * , 吕一林 1, 2 , 吴涛涛 1, 2 , 刘静 1, 2
微生物学报 | 综述 2025,65(1): 29-37
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微生物学报 | 综述 2025, 65(1): 29-37
不动杆菌属细菌中替加环素耐药基因tet(X)的研究进展
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陈冲1, 2, * , 吕一林1, 2, 吴涛涛1, 2, 刘静1, 2
作者信息
  • 1 扬州大学 农业科技发展研究院(农业与农产品安全国际联合实验室), 江苏 扬州 225009
  • 2 扬州大学 生物科学与技术学院, 江苏 扬州 225009
Research progress in tigecycline resistance genes tet(X) in Acinetobacter spp.
Chong CHEN1, 2, * , Yilin LÜ1, 2, Taotao WU1, 2, Jing LIU1, 2
Affiliations
  • 1 Institutes of Agricultural Science and Technology Development (Joint International Research Laboratory of Agriculture and Agri-product Safety), Yangzhou University, Yangzhou 225009, Jiangsu, China
  • 2 College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, Jiangsu, China
出版时间: 2025-01-04 doi: 10.13343/j.cnki.wsxb.20240439
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摘要
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不动杆菌属细菌是全球常见的条件致病菌，给人类和动物健康造成了巨大威胁。随着对碳青霉烯类抗生素耐药率的不断升高，替加环素成为治疗多重耐药不动杆菌感染的最后防线之一。近年来，替加环素耐药基因tet(X3)、tet(X4)、tet(X5)和tet(X6)等变异体的快速传播严重影响替加环素、依拉环素和奥马环素等新型四环素类抗生素的临床应用，但对不动杆菌属细菌中的tet(X)基因缺乏综述。本文通过对不动杆菌属细菌中tet(X)基因的作用机制、流行特征、传播风险和抑制剂的全面分析，进一步评估其变异体、细菌宿主、地理分布和样品来源多样性，同时为tet(X)阳性不动杆菌属病原菌的防控提供理论依据。

不动杆菌  /  tet(X)  /  插入序列共同区2 (ISCR2)  /  抑制剂

Acinetobacter spp. are the common opportunistic pathogens worldwide and pose a threat to the health of humans and animals. As the resistance rate to carbapenems aggravates, tigecycline has become one of the last lines for the treatment of multidrug-resistant Acinetobacter spp. infection. The rapid dissemination of tigecycline resistance genes tet(X3), tet(X4), tet(X5), tet(X6), and other variants in recent years has seriously affected the clinical application of new tetracycline antibiotics such as tigecycline, eravacycline, and omadacycline, whereas there is a lack of review on the tet(X) genes in Acinetobacter spp. This article comprehensively expounds the mechanisms of action, epidemiological characteristics, transmission risks, and inhibitors of tet(X) genes in Acinetobacter spp. and evaluates the diversity of their variants, bacterial hosts, geographical distribution, and sampling sources, aiming to provide a theoretical basis for the prevention and control of tet(X)-positive Acinetobacter spp.

Acinetobacter  /  tet(X)  /  insertion sequence common region 2 (ISCR2)  /  inhibitor
陈冲, 吕一林, 吴涛涛, 刘静. 不动杆菌属细菌中替加环素耐药基因tet(X)的研究进展. 微生物学报, 2025 , 65 (1) : 29 -37 . DOI: 10.13343/j.cnki.wsxb.20240439
Chong CHEN, Yilin LÜ, Taotao WU, Jing LIU. Research progress in tigecycline resistance genes tet(X) in Acinetobacter spp.[J]. Acta Microbiologica Sinica, 2025 , 65 (1) : 29 -37 . DOI: 10.13343/j.cnki.wsxb.20240439
正文
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不动杆菌属(Acinetobacter)细菌隶属于γ-变形菌纲(Gammaproteobacteria)的莫拉菌科(Moraxellaceae)，在自然界中广泛分布，无论活体还是非活体表面均可生长，且其基因组易发生突变和重组。1911年，该类菌株首次由Beijerinck从土壤中分离；1954年，Brisou和Prevot建议将其命名为不动杆菌[1]。目前，不动杆菌属细菌共有84个有效命名并报道的菌种，另有数十个种类有待确证(https://szu.cz/anemec，截至2024年10月19日)。根据中国典型培养物保藏中心的相关规则，对不动杆菌属菌种的拉丁名称进行中文翻译(http://cctcc.whu.edu.cn/portal/dictionary/index，截至2024年10月19日)。其中，鲍氏不动杆菌(A. baumannii)是导致院内不动杆菌感染的主要原因，乙酸钙不动杆菌(A. calcoaceticus)和利沃夫氏不动杆菌(A. lwoffii)等菌种引起的临床感染也时有发生[2]。由于细胞膜通透性和主动外排泵之间的共同作用，不动杆菌属细菌对多种抗生素具有天然耐药性(例如磷霉素、氨曲南等)[3]。同时，不动杆菌属细菌能够通过水平基因转移从其他种属细菌获得耐药基因[2]，从而导致可供选择的临床治疗药物减少。值得注意的是，不动杆菌属细菌对碳青霉烯类抗生素的耐药率不断上升(例如由blaNDM介导的碳青霉烯耐药性)，使临床医生对不动杆菌属细菌特别是鲍氏不动杆菌感染的治疗更加困难[2, 4]。
替加环素是在米诺环素基础上开发的第三代四环素类抗生素，通过抑制细菌蛋白质合成发挥功能，对革兰氏阴性菌和革兰氏阳性菌具有广谱的抗菌活性[5]。自2011年引进中国以来，替加环素被广泛应用于复杂皮肤及软组织感染、复杂腹腔内感染和社区获得性肺炎，被视为治疗多重耐药不动杆菌感染的最后防线之一[6]。近年来，替加环素耐药不动杆菌的不断出现，严重限制了替加环素的临床使用[7]。早期研究结果表明，替加环素耐药机制主要由外排泵和核糖体保护蛋白介导，不能通过水平基因转移获得[8]。随着研究的深入，国内外研究人员相继发现了可移动替加环素耐药基因tet(X3)、tet(X4)及其他变异体，这些变异体能够显著增强病原微生物特别是不动杆菌属细菌对替加环素的耐药水平，严重危害人类公共卫生安全和动物健康[9-10]。因此，本文对不动杆菌属细菌中tet(X)变异体的作用机制、分布特征、传播风险和抑制剂进行综述，以期推动对该类病原菌的系统认知和防控。
1 tet(X)基因的作用机制
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1991年，Speer等在专性厌氧脆弱拟杆菌的Tn4351和Tn4400转座子中发现了1个新型四环素耐药基因，即tet(X)[11]。tet(X)基因编码了长度为388个氨基酸的黄素依赖型单加氧酶Tet(X)，该蛋白能够在氧气和还原型辅酶Ⅱ的协助下催化四环素类抗生素羟基化，进而使得抗生素失活，但未达到美国食品药品监督管理局制订的替加环素耐药折点(≥8 μg/mL)[12]。2001年，专性厌氧多形拟杆菌的CTnDOT转座子中报道了2个tet(X)变异体，即tet(X1)与tet(X2)[13]。其中，tet(X1)基因所编码的Tet(X1)蛋白因缺少氮端的29个氨基酸而丧失降解活性，而tet(X2)基因所编码的Tet(X2)蛋白具有与Tet(X)蛋白相似的降解活性[12]。2019年，我国猪源鲍氏不动杆菌中报道了首个可移动的替加环素耐药基因tet(X3)，它所编码的Tet(X3)蛋白由底物结合区、配体结合区和碳端α-螺旋组成，Tet(X3)的四环素类抗生素耐药谱广于前期报道的Tet(X)、Tet(X1)与Tet(X2)，甚至可提高细菌对最新一代依拉环素和奥马环素的耐受性[9]。通过结构域交换和定点突变研究发现，Tet(X)同源蛋白具有6个关键的氨基酸位点，即L282、V329、A339、D340、V350和K351；相较于Tet(X2)，这些氨基酸残基的突变使Tet(X3)、Tet(X4)、Tet(X5)、Tet(X6)和Tet(X15)等变异体的降解活性显著增强[14-15]。进一步分析表明，突变的氨基酸残基不直接参与四环素类抗生素底物和黄素腺嘌呤二核苷酸配体的结合，而是通过与邻近氨基酸残基的相互作用间接改变Tet(X)蛋白的构象动力学[14]。面对抗生素大量使用所造成的抗生素选择压力，tet(X)变异体的出现能够促进不动杆菌属细菌更好地适应环境变化；另一方面，通过关键氨基酸位点研究，能够推动研发人员以此为靶点开发新型抗生素，对tet(X)阳性不动杆菌属细菌进行防控[14]。
2 tet(X)变异体的分布特征
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流行病学和系统发育研究发现，黄杆菌科细菌是四环素类抗生素耐药基因tet(X)的潜在起源[10, 16]。根据国际惯例，以2.0%的基因序列或蛋白质序列差异作为新基因命名及编号的阈值，若≥2.0%则赋予该基因新的命名[例如tet(X3)、tet(X4)、tet(X5)]；若 < 2.0%则将其视为已命名基因的变异体[例如tet(X3.3)、tet(X3.4)、tet(X3.5)][17]。目前，包括tet(X2)、tet(X3)、tet(X4)、tet(X5)、tet(X6)和tet(X15)在内的15个非重复tet(X)变异体分布在至少11个不同种类的不动杆菌(表1)，所编码的蛋白质具有相似的空间结构[10]。本文根据2.0%的阈值将不动杆菌属细菌中的15个tet(X)变异体归纳为6个类别，分别进行描述。
2.1 tet(X2)基因
tet(X2)基因全长1 167 bp，其编码蛋白与其他Tet(X)变异体蛋白序列相似度在86.3%− 94.8%之间。自首次在多形拟杆菌中报道以来，仅2023年在我国浙江省的人源样本中报道了1株tet(X2)阳性皮氏不动杆菌(A. pittii)[18]。
2.2 tet(X3)基因及变异体
tet(X3)基因全长1 167 bp，其编码蛋白与其他Tet(X)变异体蛋白序列相似度在79.9%−86.8%之间。2019年以来，国内外研究人员在鲍氏不动杆菌、约氏不动杆菌(A. johnsonii)、栖鱼不动杆菌(A. piscicola)、汤氏不动杆菌(A. towneri)、印度不动杆菌(A. indicus)、利沃夫氏不动杆菌、申氏不动杆菌(A. schindleri)、根特不动杆菌(A. gandensis)、诊所不动杆菌(A. nosocomialis)、皮氏不动杆菌和可变不动杆菌(A. variabilis) 等11个不动杆菌属细菌中均发现了tet(X3)基因[9-10, 19-21]。统计数据表明，tet(X3)基因是不动杆菌属细菌中的主要tet(X)亚型(4.9%)，宿主菌中印度不动杆菌和汤氏不动杆菌占比较高(17.0%)，产碳青霉烯酶NDM-1的印度不动杆菌、申氏不动杆菌和约氏不动杆菌也有检出[9-10, 21]。就样品来源而言，动物源(5.4%)和环境源(4.9%)样品中tet(X3)阳性不动杆菌属细菌的检出率显著高于人源样品(0.1%)[10]。就地理位置而言，tet(X3)阳性菌株在我国东南部地区(如广东省、江苏省)分布较多，而其他国家仅科特迪瓦和哥伦比亚等零星检出[9-10, 19]。此外，我国广西壮族自治区的1株猪源可变不动杆菌和鸡源申氏不动杆菌分别检出了tet(X3.3)−tet(X3.6)和tet(X3.7)−tet(X3.9)[20]。其中，tet(X3.3)、tet(X3.4)、tet(X3.5)、tet(X3.6)和tet(X3.8)因碱基对缺失发生移码突变，不能编码完整的蛋白质而丧失四环素类抗生素降解功能。
2.3 tet(X4)基因
tet(X4)基因全长1 158 bp，其编码蛋白与其他Tet(X)变异体蛋白序列相似度在86.1%−97.3%之间。2019年，我国研究人员首次在大肠杆菌中发现了tet(X4)基因[9]。随后，从鲍氏不动杆菌、印度不动杆菌和汤氏不动杆菌中也检测出tet(X4)基因，其来源分别为我国吉林省住院病人、青海省迁徙候鸟以及河南省猪源样本[9-10, 22]。
2.4 tet(X5)基因及变异体
tet(X5)基因全长1 167 bp，其编码蛋白与其他Tet(X)变异体蛋白序列相似度在84.9%−95.6%之间。2019年，我国研究人员首次在人源鲍氏不动杆菌发现新的tet(X)变异体，即tet(X5)[23]。随后，我们在不同来源样本(鸡和鸭等)中同样检测到携带tet(X5)基因的鲍氏不动杆菌[6]。此外，我国广西壮族自治区的猪源印度不动杆菌中报道了其变异体，即tet(X5.4)[19]。
2.5 tet(X6)基因及变异体
tet(X6)基因全长1 137 bp，与tet(X5.2)基因为同一变异体的重复命名，其编码蛋白与其他类别中Tet(X)变异体蛋白序列相似度在79.6%− 94.7%之间。2020年，我国研究人员首次在变形杆菌属细菌报道了tet(X6)基因[28]。目前，该基因已在鲍氏不动杆菌、印度不动杆菌、可变不动杆菌、汤氏不动杆菌、约氏不动杆菌、利沃夫氏不动杆菌和申氏不动杆菌中检出[6, 10, 19, 24-26]。研究表明，不动杆菌属细菌中tet(X6)基因的检出率仅次于tet(X3)，并且通常与tet(X3)基因共存于同一菌株[10]。其地理位置主要分布在中国江苏、广东和台湾等11个省份[6, 10, 19, 24-26]。此外，从我国广东省的鸡源blaNDM-1阳性鲍氏不动杆菌中检出了1个tet(X6)基因的变异体，与栖鱼不动杆菌中检出的tet(X5.3)基因为同一变异体的重复命名[10, 24]。
2.6 tet(X15)基因
tet(X15)基因全长1 158 bp，其编码蛋白与其他Tet(X)变异蛋白序列相似度在83.9%−97.3%之间。截至目前，仅2021年在我国江苏省的鸡源样本中报道了1株携带该变异体的可变不动杆菌[27]。
3 tet(X)基因的水平传播机制
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研究表明，质粒与插入序列共同区2 (insertion sequence common region 2, ISCR2)对不动杆菌属细菌中tet(X)基因的水平传播发挥着至关重要的作用[10, 29]。
3.1 质粒介导的tet(X)基因水平转移
目前，不动杆菌属细菌中由质粒携带的tet(X3)、tet(X3.7)、tet(X3.8)、tet(X3.9)、tet(X5)、tet(X5.3)、tet(X5.4)与tet(X6)基因相继被报道[10, 19-20, 23]。根据复制子序列的差异性，将携带tet(X)基因的不动杆菌属质粒划分为6个类别，即GR26、GR31、GR41、GR59、GR60和GR61[29]。体外接合转移研究表明，质粒介导的tet(X)基因水平转移事件鲜有发生，仅个别菌株可向贝氏不动杆菌(A. baylyi)和鲍氏不动杆菌进行接合转移，效率约为10−10−10−6[9-10, 19-20, 29]，并对宿主菌的生长速率造成适应性代价。Chen等研究数据显示，不动杆菌属质粒复杂多样，只有21.7%的质粒携带接合转移基因[29]。因此，质粒介导的tet(X)基因水平转移能力偏低甚至丧失，可能与质粒中接合转移元件的缺失有关，具体机制仍有待进一步探究。
3.2 插入序列ISCR2介导的tet(X)基因水平转移
ISCR2是一种类似于IS91家族的非典型插入序列，全长为1 494 bp，缺少传统的末端反向重复序列，在插入位点也不会产生同向重复序列，通常认为该序列是由复制起点oriIS向随机的复制终点terIS进行“滚环”复制，进而参与多种抗生素耐药基因的水平转移[30]。除了插入序列ISAba1介导的tet(X2)和tet(X15)基因水平转移之外，不动杆菌属细菌中tet(X3)、tet(X4)、tet(X5)和tet(X6)及变异体水平传播均与ISCR2密切相关，转座效率达到10−8−10−6，推测该插入序列是参与tet(X)基因水平传播的关键元件[6, 10, 18, 27, 31]。其中，tet(X3)基因典型的基因环境为ISCR2-tpnF-tet(X3)-hp-hp-ISCR2，上游ISCR2常被插入序列IS26或ISAba14截断[10]；tet(X4)基因在不动杆菌属细菌与大肠杆菌、肺炎克雷伯菌等肠杆菌科细菌中具有高度相似的基因环境，即ISCR2-catD-tet(X4)-ISCR2，具有跨种属传播的风险[10]；tet(X5)基因典型的基因环境为ISCR2-tpnF-tet(X5)-hp-hp-ISCR2[10]；tet(X6)基因在不动杆菌属细菌与变形杆菌属细菌中，基因环境相似，基本结构为ISCR2-hp- tet(X6)-hp-hp-ISCR2[6]。因此，ISCR2可作为遏制tet(X)基因水平扩散的潜在敲除靶点。
4 Tet(X)降解酶抑制剂
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由于Tet(X)蛋白是一类黄素依赖型单加氧酶，通过羟基化降解四环素类抗生素，因此，降解酶抑制剂成为治疗tet(X)阳性不动杆菌属细菌感染的有效方法之一。其中，白花丹醌、脱水四环素及半合成类似物等抑制剂表现出良好的协同效果，受到研究人员的密切关注。
4.1 白花丹醌
白花丹醌是从白花丹科植物提取的一种萘醌类次生代谢产物，具有抗菌、抗病毒、降血压和抗凝血等药理活性。2022年，国内研究证实白花丹醌通过与Tet(X3)和Tet(X4)蛋白催化口袋结合、改变其二级结构，从而抑制降解酶活性，是Tet(X)类降解酶的广谱抑制剂；白花丹醌与四环素类抗生素联用之后，对Tet(X3)和Tet(X4)阳性菌株具有协同杀菌作用[32]。tet(X4)阳性大肠杆菌小鼠全身感染模型治疗结果也显示，白花丹醌和美他环素的联合使用表现出显著的体内治疗效果，细菌载量和病理损伤显著减轻[32]。尽管白花丹醌等植物提取物为抗生素耐药病原菌感染提供了新的治疗选择，但浓度依赖性和安全性等问题有待解决，以此基础的结构改造为其进一步应用提供了可能。
4.2 脱水四环素及半合成类似物
目前，研究人员已得到多种四环素类抗生素降解酶与底物的结合模式，发现脱水四环素及类似物是Tet(X)类降解酶的广谱抑制剂[33-34]。脱水四环素是四环素的生物合成前体，结构上与四环素相似，但C6位置的脱水改变了其构象，变得更加疏水[33]。对于Tet(X)与Tet(X3)蛋白，脱水四环素、脱水金霉素与脱水地美环素等类似物具有良好的抑制作用，能够显著抑制酶蛋白对替加环素的降解活性[34]。脱水四环素与Tet(X6)蛋白的结合模型进一步表明，脱水四环素通过竞争性结合的方式，显著降低了Tet(X6)蛋白对四环素类抗生素的降解活性，并且Tet(X)同源蛋白具有保守的结合位点[35]。因此，脱水四环素及半合成类似物在四环素类抗生素抗菌增效剂方面具有广阔的应用前景。
5 展望
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总体而言，tet(X)变异体尤其是tet(X3)阳性不动杆菌属细菌在我国快速传播，它们的基因亚型、宿主范围、分布地区和样品来源呈多样化，能够显著降解包括替加环素、依拉环素和奥马环素在内的所有四环素类抗生素，进而威胁四环素类抗生素的临床应用。面对tet(X)阳性不动杆菌属细菌复杂多样的现状，传统方法已无法满足对其快速、准确鉴定的需求。随着高通量测序技术的不断成熟，全基因组测序及数据库的构建等有助于对该类菌株的监控和溯源，以便在重点环节制订针对性的干预措施。
另一方面，可移动基因元件尤其ISCR2是参与tet(X3)、tet(X4)、tet(X5)和tet(6)等tet(X)变异体水平传播的关键元件。CRISPR-Cas9技术是目前最有效的基因组编辑方法之一，能否通过构建CRISPR-Cas9基因敲除系统对ISCR2进行靶向敲除，抑制tet(X)变异体在不同菌种之间的水平转移，值得深入探究。此外，白花丹醌、脱水四环素及半合成类似物等抑制剂对tet(X)变异体的降解活性具有高效的抑制作用，与四环素类抗生素联合使用后的治疗效果得到显著改善。在我国“减抗、限抗”的政策背景下，tet(X)阳性不动杆菌属细菌的防控工作至关重要，基因敲除技术和抑制剂为降低该类菌株的临床威胁提供了新思路。
基金
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  • 国家自然科学基金(32402890)
  • 江苏省自然科学基金(BK20210803)
  • 中国博士后科学基金(2023M732993)
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doi: 10.13343/j.cnki.wsxb.20240439
  • 接收时间：2024-07-18
  • 首发时间：2026-03-21
  • 出版时间：2025-01-04
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  • 收稿日期：2024-07-18
  • 录用日期：2024-11-01
基金
National Natural Science Foundation of China(32402890)
国家自然科学基金(32402890)
Natural Science Foundation of Jiangsu Province(BK20210803)
江苏省自然科学基金(BK20210803)
China Postdoctoral Science Foundation(2023M732993)
中国博士后科学基金(2023M732993)
作者信息
    1 扬州大学 农业科技发展研究院(农业与农产品安全国际联合实验室), 江苏 扬州 225009
    2 扬州大学 生物科学与技术学院, 江苏 扬州 225009

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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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