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Article(id=1307007539380510747, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307007396681900041, articleNumber=null, orderNo=null, doi=10.11843/j.issn.0366-6964.2026.01.033, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1736352000000, receivedDateStr=2025-01-09, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1789544480413, onlineDateStr=2026-09-16, pubDate=1769097600000, pubDateStr=2026-01-23, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1789544480413, onlineIssueDateStr=2026-09-16, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1789544480413, creator=13701087609, updateTime=1789544480413, updator=13701087609, issue=Issue{id=1307007396681900041, tenantId=1146029695717560320, journalId=1306274286668972124, year='2026', volume='57', issue='1', pageStart='1', pageEnd='568', issueExtLink='null', onlineDate='null', pubDate='1769097600000', pubDateStr='2026-01-23', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1789544446392, creator='13701087609', updateTime=1789609890784, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1307281890638057732, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307007396681900041, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1307281890738721029, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307007396681900041, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=378, endPage=391, ext={EN=ArticleExt(id=1307007539581837340, articleId=1307007539380510747, tenantId=1146029695717560320, journalId=1306274286668972124, language=EN, title=Isolation， Identification and Whole Genome Sequencing Analysis of a Bovine-derived Shigella flexneri Strain, columnId=1307007432299930010, journalTitle=Acta Veterinaria et Zootechnica Sinica, columnName=PREVENTIVE VETERINARY MEDICINE, runingTitle=null, highlight=null, articleAbstract=

In recent years， diarrhea in cattle has been spreading in cattle farms with a high mortality rate， causing economic losses. This experiment aims to isolate and identify Shigella flexneri， which causes diarrhea in a Beijing cattle farm， and to clarify the biological characteristics and genomic features of the pathogen’s serotype， drug resistance， and pathogenicity. In this study， fecal samples from diarrheal cattle were collected for bacterial isolation and purification， 16S rRNA amplicon sequencing analysis， virulence gene detection， and whole-genome sequencing of isolated strains. The results showed that one strain of Shigella flexneri Fc was identified through bacterial isolation and purification， and PCR identification. Whole-genome sequencing revealed that the Shigella flexneri Fc strain has a genome size of 4.98 Mb and a GC content of 50.76%. It contains 91 tRNA genes， 7 23S rRNA， 7 16S rRNA， 8 5S rRNA， 283 misc_RNA， and 97 carbohydrate-active enzyme genes. TVBD annotation analysis identified 1 363 transporter genes； CARD annotation analysis identified 80 resistance genes； VFDB and PHI-base annotation analysis identified 1 410 potential virulence factor-related genes and 2 052 phenotypic mutation genes. Phylogenetic tree analysis revealed that Shigella flexneri is closely related to Shigella flexneri 29903， belonging to the same branch. This study completed the isolation and identification of a bovine-origin Shigella flexneri strain and whole-genome sequencing analysis， providing a theoretical basis for the prevention and control research of shigellosis.

, authors=Jing ZHANG, Yaping WANG, Xiwen FAN, Zhen WANG, authorsList=Jing ZHANG, Yaping WANG, Xiwen FAN, Zhen WANG, authorCompany=null, correspAuthors=Zhen WANG, authorNote=null, correspAuthorsNote=
WANG Zhen， E-mail：
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近年来，牛易患腹泻病在牛场中进行传播，并有着较高的致死率，造成经济损失。本试验旨在对引起北京某牛场牛腹泻的福氏志贺菌进行分离鉴定，明确病原菌的血清型、耐药性和致病性等生物学特性及基因组特征。本研究采集腹泻牛粪便样本，进行细菌分离纯化、16S rRNA扩增子测序分析、毒力基因检测和分离株全基因组测序。结果显示，经细菌分离纯化、PCR鉴定发现一株福氏志贺菌Fc；基因组测序获得福氏志贺菌株Fc株全基因组大小为4.98 Mp，GC含量为50.76%；含有91个tRNA基因，7个23S rRNA，7个16S rRNA，8个5S rRNA，283个misc_RNA，97个碳水化合物活性酶基因；TVBD注释分析发现1 363个转运蛋白基因；CARD注释分析发现80个抗性基因；VFDB和PHI-base注释分析发现1 410个潜在的毒力因子相关基因及2 052个表型突变基因等。系统进化树分析发现福氏志贺菌与福氏志贺菌29903属于同一分支，进化关系最近。本研究完成了一株牛源福氏志贺菌的分离鉴定和全基因组测序分析，为志贺氏菌病的防控研究提供了理论依据。

, authors=张晶, 王亚平, 樊曦雯, 王真, authorsList=张晶, 王亚平, 樊曦雯, 王真, authorCompany=null, correspAuthors=王真, authorNote=

张晶，硕士，主要从事预防兽医学研究，E-mail：

, correspAuthorsNote=
王真，主要从事动物疫病防控技术、细菌致病及耐药机制研究，E-mail：
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张晶，硕士，主要从事预防兽医学研究，E-mail：

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张晶，硕士，主要从事预防兽医学研究，E-mail：

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companyId=1307286634219728919, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=北京农学院动物科学技术学院，兽医学（中兽医）北京市重点实验室，北京 102206)])], figs=[ArticleFig(id=1307286638174957622, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Fig.1, caption=Agarose gel electrophoresis of PCR products of 16S rRNA gene of isolate

M. DL5000 DNA standard； 1. 16S rRNA PCR amplification； 2. Blank control

, figureFileSmall=N30xE4JZ2YndEybouaQC5A==, figureFileBig=hw6zscvSITZRF/U8i6dwkg==, tableContent=null), ArticleFig(id=1307286638250455095, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=图1, caption=分离菌16S rRNA基因PCR产物琼脂糖凝胶电泳图

M．DL5000 DNA相对分子质量标准；1. 16S rRNA PCR扩增；2.空白对照

, figureFileSmall=N30xE4JZ2YndEybouaQC5A==, figureFileBig=hw6zscvSITZRF/U8i6dwkg==, tableContent=null), ArticleFig(id=1307286638393061432, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Fig.2, caption=Shigella flexneri Fc strain whole genome circle map

From the outside to the inside， the circles are as follows： The first circle represents the genomic coordinates； the second circle shows genes on the positive strand of the genome sequence， with different colors indicating different COG functional categories； the third circle displays genes on the negative strand of the genome sequence， again with different colors for different COG functional categories； the fourth circle marks the locations of rRNA and tRNA on the genome sequence， with rRNA in blue and tRNA in red； the fifth circle illustrates the GC content curve of the genome sequence， calculated by sliding a 2000bp window across the genome and averaging the GC content； the sixth circle depicts the GC skew curve of the genome sequence， also determined by sliding a 2000bp window across the genome and calculating the GC skew， with green representing G content

, figureFileSmall=PUqhPnn+yeDorzz07S93vg==, figureFileBig=zQHVvq6Puruqdcw8Ynx88A==, tableContent=null), ArticleFig(id=1307286638464364601, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=图2, caption=福氏志贺菌Fc株的全基因组图谱

由外到内依次：第一圈，基因组坐标；第二圈，基因组序列正链上的基因，不同颜色代表不同的COG功能分类；第三圈，基因组序列负链上的基因，不同颜色代表不同的COG功能分类；第四圈，基因组序列上的rRNA和tRNA，rRNA是蓝色，tRNA是红色；第五圈，基因组序列的GC含量曲线，以2 000 bp为一滑窗在基因组上滑动，统计的平均GC含量；第六圈，基因组序列的GC skew曲线，以2 000 bp为一滑窗在基因组上滑动，统计GC skew；绿色表示G含量

, figureFileSmall=PUqhPnn+yeDorzz07S93vg==, figureFileBig=zQHVvq6Puruqdcw8Ynx88A==, tableContent=null), ArticleFig(id=1307286638527279162, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Fig.3, caption=Species distribution map of the NR in Shigella flexneri Fc strain genome, figureFileSmall=Z8SfSYtPPyoMyTQacGmOOw==, figureFileBig=hec+mRi+m2MxDaZujp4iBA==, tableContent=null), ArticleFig(id=1307286638585999419, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=图3, caption=福氏志贺氏菌Fc株基因组的NR物种分布图, figureFileSmall=Z8SfSYtPPyoMyTQacGmOOw==, figureFileBig=hec+mRi+m2MxDaZujp4iBA==, tableContent=null), ArticleFig(id=1307286638653108284, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Fig.4, caption=COG functional categories map of the Shigella flexneri genome, figureFileSmall=BbDHPkkOn1zeCkkwlEOXWw==, figureFileBig=w4swENumTgj9BGUCwdZ2dg==, tableContent=null), ArticleFig(id=1307286638716022845, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=图4, caption=福氏志贺菌基因组COG 功能分类图, figureFileSmall=BbDHPkkOn1zeCkkwlEOXWw==, figureFileBig=w4swENumTgj9BGUCwdZ2dg==, tableContent=null), ArticleFig(id=1307286638791520318, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Fig.5, caption=Classification diagram of KEGG metabolic pathway of the Shigella flexneri genome

The x-axis represents the number of annotated genes under Pathway classification； the y-axis represents the Pathway categories， with different colors indicating their respective major classifications

, figureFileSmall=KeItF26bCAhV8AVsvUyeAw==, figureFileBig=tepyzrEY7O/Mn7JSYL7sSw==, tableContent=null), ArticleFig(id=1307286638871212095, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=图5, caption=福氏志贺菌基因组的KEGG代谢通路分类图

横坐标为 Pathway 分类下注释的基因数目；纵坐标为 Pathway 分类，不同颜色代表所属的不同的大分类

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Primers for PCR identification of Shigella flexneri

, figureFileSmall=null, figureFileBig=null, tableContent=

基因名称

Gene name

引物序列（5′→3′）

Primer sequences

片段大小/bpFragment length/bp
16S rRNATGGCTCAGATTGAACGCTGG1 488
TACCTTGTTACGACTTCAC
), ArticleFig(id=1307286641048055880, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=表1, caption=

福氏志贺菌PCR鉴定引物表

, figureFileSmall=null, figureFileBig=null, tableContent=

基因名称

Gene name

引物序列（5′→3′）

Primer sequences

片段大小/bpFragment length/bp
16S rRNATGGCTCAGATTGAACGCTGG1 488
TACCTTGTTACGACTTCAC
), ArticleFig(id=1307286641110970441, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Table 1, caption=

Statistics of gene prediction results

, figureFileSmall=null, figureFileBig=null, tableContent=

类型

Type

数量

Number

总长度

Total length

平均长度

Average length

基因组比例/%

Percentage of genome （%）

Gene5 7505 006 97187188.63
CDS5 3534 934 75792287.36
tRNA917 137780.13
23S rRNA720 3142 9020.36
16S rRNA710 7661 5380.19
5S rRNA88881110.02
tmRNA13633630.01
misc_RNA28332 7461160.58
), ArticleFig(id=1307286641199050826, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=表1, caption=

基因预测结果统计

, figureFileSmall=null, figureFileBig=null, tableContent=

类型

Type

数量

Number

总长度

Total length

平均长度

Average length

基因组比例/%

Percentage of genome （%）

Gene5 7505 006 97187188.63
CDS5 3534 934 75792287.36
tRNA917 137780.13
23S rRNA720 3142 9020.36
16S rRNA710 7661 5380.19
5S rRNA88881110.02
tmRNA13633630.01
misc_RNA28332 7461160.58
), ArticleFig(id=1307286641287131211, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Table 2, caption=

Result of CAZy

, figureFileSmall=null, figureFileBig=null, tableContent=
分类 Class数量 Number说明 Descrition
糖苷水解酶GHs42Glycoside hydrolases
糖基转移酶GTs36Glycosy transferases
多糖裂合酶PLs0Polysaccharide lyases
碳水化合物酯酶CEs8Carbohydrate esterases
辅助氧化还原酶AAs3Auxiliary activities
碳水化合物结合模块CBMs3Carbohydrate-binding modules
), ArticleFig(id=1307286641366822988, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=表2, caption=

碳水化合物活性酶统计结果

, figureFileSmall=null, figureFileBig=null, tableContent=
分类 Class数量 Number说明 Descrition
糖苷水解酶GHs42Glycoside hydrolases
糖基转移酶GTs36Glycosy transferases
多糖裂合酶PLs0Polysaccharide lyases
碳水化合物酯酶CEs8Carbohydrate esterases
辅助氧化还原酶AAs3Auxiliary activities
碳水化合物结合模块CBMs3Carbohydrate-binding modules
), ArticleFig(id=1307286641438126157, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Table 3, caption=

Virulence factors in Shigella flexneri Fc strain genome

, figureFileSmall=null, figureFileBig=null, tableContent=

毒力因子

Virulence factors

相关基因数

Related genes number

硝酸还原酶 Nitrate reductase27
周毛鞭毛 Peritrichous flagella59
荚膜 Capsule68
寡聚糖 LOS42
O抗原 O-antigen23
脂多糖 LPS27
IV型菌毛 Type IV pili39
), ArticleFig(id=1307286641505235022, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=表3, caption=

福氏志贺菌Fc株中的毒力因子

, figureFileSmall=null, figureFileBig=null, tableContent=

毒力因子

Virulence factors

相关基因数

Related genes number

硝酸还原酶 Nitrate reductase27
周毛鞭毛 Peritrichous flagella59
荚膜 Capsule68
寡聚糖 LOS42
O抗原 O-antigen23
脂多糖 LPS27
IV型菌毛 Type IV pili39
), ArticleFig(id=1307286641580732495, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=EN, label=Table 4, caption=

Prediction of antibiotic resistance genes in Shigella flexneri Fc strain

, figureFileSmall=null, figureFileBig=null, tableContent=

耐药机制

Resistance Mechanism

抗生素耐药基因数

Antibiotic resistance genes number

抗性

Resistances

抗生素外排泵

Antibiotic efflux

45氟喹诺酮类、头孢菌素类、头霉素类、青霉烷类、大环内酯类、磷霉素、硝基咪唑类、四环素类、肽类、氨基糖苷类、核苷类、磺胺类抗生素

抗生素失活

Antibiotic inactivation

17β-内酰胺类、林可酰胺类、氟喹诺酮类、四环素类、利福霉素类抗生素

抗生素靶标改变

Antibiotic target alteration

14肽类、氟喹诺酮类、头孢菌素类、甘氨酰环素类、青霉烷类、四环素类、利福霉素类、苯酚类、三氯生、头霉素类、青霉烷类抗生素

抗生素靶标保护

Antibiotic target protection

2氟喹诺酮类抗生素

抗生素靶标替换

Antibiotic target replacement

2复合磺胺类、磺胺二甲氧嘧啶
), ArticleFig(id=1307286641647841360, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307007539380510747, language=CN, label=表4, caption=

福氏志贺菌Fc株中的耐药基因

, figureFileSmall=null, figureFileBig=null, tableContent=

耐药机制

Resistance Mechanism

抗生素耐药基因数

Antibiotic resistance genes number

抗性

Resistances

抗生素外排泵

Antibiotic efflux

45氟喹诺酮类、头孢菌素类、头霉素类、青霉烷类、大环内酯类、磷霉素、硝基咪唑类、四环素类、肽类、氨基糖苷类、核苷类、磺胺类抗生素

抗生素失活

Antibiotic inactivation

17β-内酰胺类、林可酰胺类、氟喹诺酮类、四环素类、利福霉素类抗生素

抗生素靶标改变

Antibiotic target alteration

14肽类、氟喹诺酮类、头孢菌素类、甘氨酰环素类、青霉烷类、四环素类、利福霉素类、苯酚类、三氯生、头霉素类、青霉烷类抗生素

抗生素靶标保护

Antibiotic target protection

2氟喹诺酮类抗生素

抗生素靶标替换

Antibiotic target replacement

2复合磺胺类、磺胺二甲氧嘧啶
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一株牛源福氏志贺菌的分离鉴定及全基因组测序分析
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张晶 , 王亚平 , 樊曦雯 , 王真
畜牧兽医学报 | 预防兽医 2026,57(1): 378-391
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畜牧兽医学报 |预防兽医 2026 , 57 (1) : 378 -391
一株牛源福氏志贺菌的分离鉴定及全基因组测序分析
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张晶 , 王亚平, 樊曦雯, 王真
作者信息
  • 北京农学院动物科学技术学院，兽医学（中兽医）北京市重点实验室，北京 102206
通讯作者:
王真，主要从事动物疫病防控技术、细菌致病及耐药机制研究，E-mail：
作者简介:

张晶，硕士，主要从事预防兽医学研究，E-mail：

Isolation， Identification and Whole Genome Sequencing Analysis of a Bovine-derived Shigella flexneri Strain
Jing ZHANG , Yaping WANG, Xiwen FAN, Zhen WANG
Affiliations
  • Beijing Key Laboratory of Traditional Chinese Veterinary Medicine，Animal Science and Technology College，Beijing University of Agriculture，Beijing 102206，China
    • Corresponding Author:
    WANG Zhen， E-mail：
出版时间: 2026-01-23 doi: 10.11843/j.issn.0366-6964.2026.01.033
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摘要
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近年来，牛易患腹泻病在牛场中进行传播，并有着较高的致死率，造成经济损失。本试验旨在对引起北京某牛场牛腹泻的福氏志贺菌进行分离鉴定，明确病原菌的血清型、耐药性和致病性等生物学特性及基因组特征。本研究采集腹泻牛粪便样本，进行细菌分离纯化、16S rRNA扩增子测序分析、毒力基因检测和分离株全基因组测序。结果显示，经细菌分离纯化、PCR鉴定发现一株福氏志贺菌Fc；基因组测序获得福氏志贺菌株Fc株全基因组大小为4.98 Mp，GC含量为50.76%；含有91个tRNA基因，7个23S rRNA，7个16S rRNA，8个5S rRNA，283个misc_RNA，97个碳水化合物活性酶基因；TVBD注释分析发现1 363个转运蛋白基因；CARD注释分析发现80个抗性基因；VFDB和PHI-base注释分析发现1 410个潜在的毒力因子相关基因及2 052个表型突变基因等。系统进化树分析发现福氏志贺菌与福氏志贺菌29903属于同一分支，进化关系最近。本研究完成了一株牛源福氏志贺菌的分离鉴定和全基因组测序分析，为志贺氏菌病的防控研究提供了理论依据。

福氏志贺菌  /  全基因组测序  /  耐药性  /  毒力

In recent years， diarrhea in cattle has been spreading in cattle farms with a high mortality rate， causing economic losses. This experiment aims to isolate and identify Shigella flexneri， which causes diarrhea in a Beijing cattle farm， and to clarify the biological characteristics and genomic features of the pathogen’s serotype， drug resistance， and pathogenicity. In this study， fecal samples from diarrheal cattle were collected for bacterial isolation and purification， 16S rRNA amplicon sequencing analysis， virulence gene detection， and whole-genome sequencing of isolated strains. The results showed that one strain of Shigella flexneri Fc was identified through bacterial isolation and purification， and PCR identification. Whole-genome sequencing revealed that the Shigella flexneri Fc strain has a genome size of 4.98 Mb and a GC content of 50.76%. It contains 91 tRNA genes， 7 23S rRNA， 7 16S rRNA， 8 5S rRNA， 283 misc_RNA， and 97 carbohydrate-active enzyme genes. TVBD annotation analysis identified 1 363 transporter genes； CARD annotation analysis identified 80 resistance genes； VFDB and PHI-base annotation analysis identified 1 410 potential virulence factor-related genes and 2 052 phenotypic mutation genes. Phylogenetic tree analysis revealed that Shigella flexneri is closely related to Shigella flexneri 29903， belonging to the same branch. This study completed the isolation and identification of a bovine-origin Shigella flexneri strain and whole-genome sequencing analysis， providing a theoretical basis for the prevention and control research of shigellosis.

Shigella flexneri  /  whole-genome sequencing  /  drug resistance  /  virulence
张晶, 王亚平, 樊曦雯, 王真. 一株牛源福氏志贺菌的分离鉴定及全基因组测序分析. 畜牧兽医学报, 2026 , 57 (1) : 378 -391 . DOI: 10.11843/j.issn.0366-6964.2026.01.033
Jing ZHANG, Yaping WANG, Xiwen FAN, Zhen WANG. Isolation， Identification and Whole Genome Sequencing Analysis of a Bovine-derived Shigella flexneri Strain[J]. Acta Veterinaria et Zootechnica Sinica, 2026 , 57 (1) : 378 -391 . DOI: 10.11843/j.issn.0366-6964.2026.01.033
正文
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志贺菌是临床上最常见的肠道病原体之一，主要分为4种血清群：痢疾志贺菌、福氏志贺菌、鲍氏志贺菌和宋内志贺菌。其中福氏志贺菌（Shigella flexneri，S. flexneri）是发展中国家的主要血清群，是一种兼性厌氧菌的革兰阴性杆菌和重要的人类适应性病原体，也是导致人类细菌性痢疾的主要流行菌型，根据抗原不同分为13个血清型［1］，其中常见的有1b型、2a型、3a型和4型。志贺菌感染力强，由于抗生素的滥用导致耐药性严重，出现多重耐药菌株［2］，且没有有效的疫苗［3］，可引起腹泻和发热性痢疾，包括人类溶血性结肠炎和出血性尿毒症综合征，严重者可出现神经症状和伴发败血症。志贺菌自然宿主通常是人类和其他灵长类动物，每年导致约21.6万人死亡［4］。近年来，牛、猴、兔、犊牛、鱼、鸡和仔猪均有感染志贺菌的报道［5］。
S. flexneri属于侵袭性细菌，S. flexneri引起的细菌性痢疾为志贺氏菌病，是导致5岁以下儿童中患腹泻死亡的第二大原因［6］，主要通过细胞内增殖和胃肠道上皮细胞机制引起人类的轻度腹泻［7］，由效应物递送系统（T3SS和T6SS）、不同的蛋白质效应物、毒素、铁摄取基因等介导［8］。志贺菌在侵袭宿主时，产生的多种毒力因子发挥了重要作用，如志贺毒素、志贺菌肠毒素、超氧化物酶歧化酶、表面膜蛋白和菌毛等。因此，对分离出的S. flexneri毒力基因携带情况进行分析可为致病性分析提供基本参考。PCR和ELISA是目前实验室中较常用于检测腹泻病原微生物的两种方法，不仅检测准确、迅速，而且适用范围广。
对于志贺菌感染的免疫保护作用主要是针对细菌脂多糖中的O特定多糖组分，理想的多价志贺菌疫苗应针对全球最常见的志贺菌种和多种血清型［9］。为加强对福氏志贺菌感染后毒力基因和耐药基因的理解，全基因组测序是必不可少的手段。本研究了解到北京地区某牛场出现发热咳嗽、呼吸困难和腹泻的病牛，试验采集了病牛的鼻咽拭子与粪便组织病料，通过分离纯化、耐药性和16S rRNA全基因测序，分离鉴定出一株福氏志贺菌，并对其进行毒力基因检测和全基因组测序分析，以期为志贺菌病防控技术研究提供理论基础。
1　材料与方法
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1.1　试剂
TSB培养基、SS琼脂培养基、MH培养基和细菌生化鉴定管购自青岛海博生物科技有限公司；2×SanTaq PCR Mix和DL5000 DNA Marker购自生工生物工程股份有限公司；AidRed（GelRed）核酸染料购自北京艾德莱生物有限公司；引物由北京擎科生物科技有限公司合成；抗生素药敏纸片购自杭州天和微生物试剂有限公司。
1.2　细菌分离培养
将粪便样品（北京小段奶牛合作社中出现发热咳嗽、呼吸困难和腹泻的病牛）涂布于SS平板，37 ℃培养24 h。挑取单菌落，接种到TSB液体培养基中，200 r·min-1，37 ℃培养12 h，重新在SS平板上划线，24 h后观察菌落特征。
1.3　分离菌16S rRNA PCR鉴定
参照GenBank中福氏志贺菌的16S rRNA基因序列设计引物，引物序列见表1，用2×SanTaq PCR Mix体系进行PCR扩增，PCR反应体系（20 µL）：模板2 µL，上、下游引物各0.5 µL，ddH2O 7 µL，2×SanTaq PCR Mix 10 µL。PCR反应程序设置：94 ℃预变性5 min；94 ℃变性30 s，56 ℃退火30 s，72 ℃延伸1 min，共30个循环；72 ℃延伸10 min。取PCR扩增产物进行1%琼脂糖凝胶电泳（110 V电泳30 min），在凝胶成像系统成像，观察记录结果，将PCR产物送去北京擎科生物有限公司进行测序，测序结果在NCBI数据库进行BLAST比对。
1.4　分离菌的药敏试验
选取福氏志贺菌为研究对象，进行耐药性分析。参照美国临床和实验室标准协会（CLSI）推荐的操作，采用K-B（Kirby-Bauer）药敏纸片扩散法［10］，用27种临床常用广谱抗生素药敏片对福氏志贺菌进行药物敏感试验。依据CLSI中抑菌直径解释标准进行敏感、中度敏感和耐药的结果判读。抗菌药物包括β-内酰胺类（青霉素G、阿莫西林、氨苄西林、羧苄西林、头孢噻肟、头孢克肟、头孢噻吩和亚胺培南）、大环内酯类（红霉素和阿奇霉素）、氨基糖苷类（链霉素、卡那霉素、新霉素和阿米卡星）、四环素类（四环素、强力霉素和米诺环素）、喹诺酮类（诺氟沙星、左氧氟沙星和环丙沙星）、多肽类（万古霉素和多黏菌素B）、酰胺醇类（氯霉素和氟苯尼考）、磺胺类（复方新诺明）、利福霉素类（利福平）和林可霉素类（克林霉素）抗生素。
培养福氏志贺菌病原菌菌液，将其浓度调整为0.5麦氏浊度，在生物安全柜中进行操作，取各组菌液100 μL滴于MH固体培养基上，用灭菌的玻璃棒在平皿上均匀涂抹整个琼脂表面，置室温3~5 min，用无菌镊子取药敏纸片，贴于平板表面，置于37 ℃温箱培养16~18 h量取抑菌圈直径，记录药敏结果。
1.5　分离菌的全基因组测序
取-80 ℃保存的分离菌甘油管，使用涂布棒将分离菌用平板划线法连续在SS培养基纯化培养3代后，挑取单菌落在TSB中培养到对数期，8 000 r·min-1离心10 min收集菌体，由北京奥维森基因科技有限公司提取细菌基因组DNA并进行全基因组测序，采用三代Nanopore进行建库测序，样品检测和纯化后使用SQK-LSK110试剂盒并按照说明书构建1D文库，同时使用VAHTS® Universal Plus DNA Library Prep Kit for MGI V2/for illumia V2试剂构建小片段文库，文库质检合格后使用Nanopore PromethION和Illumina NovaSeq 6000平台进行测序。
1.6　分离菌的全基因组分析
利用PlasFlow软件对细菌基因组组装结果进行质粒的鉴定，对获得的质粒序列利用BLAST软件和PLSDB数据库进行质粒注释；使用BWA（Ver 0.7.17-r1188）软件将illumina短序列与拼接完成的基因组进行比对完成二代测序深度统计，三代测序深度统计使用Minimap2（Ver 2.24-r1122）［11］将长序列与拼接完成的基因组进行比对；然后使用Samtools（Ver 1.15.1）depth［12］工具，统计二、三代测序数据的平均测序深度，反应不同区域的reads覆盖情况。
使用mlst（Version：2.23.0）进行多位点序列分型（Multilocus sequence typing，MLST），使用Prokka（Version：1.14.6）［13］对组装后的基因组进行编码基因预测。为全面分析福氏志贺菌的基因功能信息，对八大数据库的基因功能进行注释，包括：UniProt［14］、Kyoto encyclopedia of genes and genomes（KEGG）［15］及KEGG Pathway、gene ontology（GO）［16］、Pfam［17］、cluster of orthologous groups of proteins（COG）［18］、RefSeq、non-redundant protein database（NR）。将预测得到的基因序列与COG、KEGG、Uniprot、Refseq等功能数据库做BLAST比对，得到基因功能注释结果，使用hmmer基于Pfam和TIGERFAM数据库进行功能注释。
使用diamond基于抗性基因数据库（Antibiotic Resistance Genes Database，ARDB）［19］对福氏志贺菌的蛋白质序列进行注释；使用hmmer对碳水化合物活性酶数据库（Carbohydrate-active enzymes database，CAZy）的蛋白质序列进行注释分析化合物酶的基因组、结构和生物化学信息；使用blastp对综合抗生素耐药性数据库（The Comprehensive Antibiotic Resistance Database，CARD）［20］注释耐药基因和抗性机制以及对毒力因子数据库（Virulence Factors Database，VFDB）的福氏志贺菌毒力基因进行注释；使用diamond blastp对膜转运蛋白分类数据库（Transporter Classification Database， TCBD）对膜转运蛋白进行注释；使用EffectiveT3（Version：2.0.2）预测Ⅲ型分泌系统（type Ⅲ secretion system，T3SS）对T3SS蛋白进行注释。
1.7　系统进化树分析
将福氏志贺菌的16S rRNA基因序列在NCBI上进行BLAST比对，从中挑选20条不同地区的高同源性序列，利用MEGA 11中Neighbor-Joining法构建系统进化树。
2　结果
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2.1　细菌分离纯化和PCR鉴定结果
从组织病料分离出疑似福氏志贺菌，菌落形态在SS固体培养基上形成圆形和边缘光滑整齐的小菌落。分离菌株经福氏志贺菌的16S rRNA引物扩增，琼脂糖凝胶电泳后扩增结果如图1所示，分离菌扩增出了与预期片段大小一致1 488 bp的目的基因。通过BLAST比对分析，其与福氏志贺菌的相似度>99.8%，确定分离菌株并命名为福氏志贺菌Fc株。
2.2　福氏志贺菌的耐药表型分析
对福氏志贺菌Fc株进行药敏试验，福氏志贺菌对20种抗生素耐药，包括9类抗生素：β-内酰胺类（青霉素G、阿莫西林、氨苄西林、羧苄西林、头孢噻肟、头孢克肟、头孢噻吩和亚胺培南）、大环内酯类（红霉素）、氨基糖苷类（链霉素、卡那霉素、新霉素）、四环素类（四环素和强力霉素）、多肽类（万古霉素）、酰胺醇类（氯霉素和氟苯尼考）、磺胺类（复方新诺明）、利福霉素类（利福平）和林可霉素类（克林霉素）抗生素。结果表明，福氏志贺菌Fc株是多重耐药病原菌。
2.3　分离菌福氏志贺菌Fc株的全基因组测序
对基因组结构注释信息、GC分布及基因组COG功能注释进行整合，绘制基因组圈图如图2所示，circlize可视化基因组，测序得到福氏志贺菌Fc株全基因组大小为4.98 Mb，GC的平均含量为50.76%，具体编码基因预测结果如表1所示，所有编码基因的总长度为5 006 971 bp，编码的基因为5 750个，平均长度为871 bp，编码基因总长度占全基因的88.63%，含有91个tRNA基因，7个23S rRNA，7个16S rRNA，8个5S rRNA，283个misc_RNA。
2.4　蛋白编码基因与功能注释
2.4.1　蛋白编码基因的NR注释和COG注释
福氏志贺菌Fc株中有5 350个基因在NR数据库中得到注释，NR数据库是非冗余蛋白质的氨基酸序列数据库，包含SwissProt、PIR（Protein Information Resource）、PRF（Protein Research Foundation）、PDB（Protein Data Bank）蛋白质数据库非冗余的数据以及从GenBank和RefSeq的CDS数据翻译来的蛋白质数据，NR物种分布如图3所示，福氏志贺菌属于肠杆菌科，物质分类分别为肠杆菌科Enterobacteriaceae（46.38%）、Escherichia（24.87%）、Escherichia coli（12.69%）、Bacteria（6.11%）、Enterobacterales（4.57%）、Gammaproteobacteria（3.06%）、Proteobacteria（0.93%）、Escherichia coli MS 198-1（0.55%）、Escherichia coli FVEC1412（0.45%）和Escherichia coli KTE228（0.38%）。
对菌株福氏志贺菌Fc株基因组中编码功能性蛋白的基因进行COG注释，COG是对基因产物进行直系同源分类的数据库，发现被注释到具有生物学活性的蛋白编码基因共4 934个，结果如图4所示，基因功能注释信息分为24类，较丰富的几个类别依次是碳水化合物运输和代谢（carbohydrate transport and metabolism）共443个基因，氨基酸代谢及转运（amino acid transport and metabolism）共431个基因，转录（transcription）共360个基因，仅用于一般功能预测（general function prediction only）共358个基因，细胞壁/膜/包膜生物发生（cell wall/membrane/envelope biogenesis）共337个基因，而关于无机离子转运与代谢（lnorganic ion transport and metabolism）共有312个基因，能量生产和转换（energy production and conversion）共296个基因，翻译、核糖体结构和生物发生（translation， ribosomal structure and biogenesis）共264个基因，信号传导机制（signal transduction mechanisms）共235个基因。此外，还有186个基因尚未确定功能，这些基因可能赋予菌株某些特殊的生物学功能，有待今后进一步的研究。这些有大量基因富集的功能，对于维持细菌正常生命活动必不可少。
2.4.2　福氏志贺菌Fc株基因序列的KEGG和GO注释
将菌株福氏志贺菌Fc株所获得的基因组信息与KEGG数据库进行比对并分析，KEGG是通过系统分析细菌的基因产物在细胞中的代谢途径以及这些基因产物功能的主要公共数据库，如图5示，3 893个基因对应到KEGG通路，富集在23条代谢通路中。KEGG富集分析显示，全局和概述图（global and overview maps）、膜传输（membrane transpart）、氨基酸代谢（amino acid metabolism）和碳水化合物代谢（carbohydrate metabolism）通路注释基因是最多的，分别有1 019、363、291和223个基因注释；此外，辅助因子和维生素的代谢（metabolism of cofactors and vitamins）、信号转导（signal transduction）、能量代谢（energy metabolism）等通路也具有较高相关度。
GO是一个国际标准化的基因功能分类体系，包括一套动态更新的标准词汇表来全面描述生物体中基因和基因产物的属性。将GO注释信息经简化后得到GOslim分类，将基因的功能从生物过程（biological process，BP）、细胞组分（cellular component，CC）和分子功能（molecular function，MF）对蛋白进行注释，选取每个分类下前20个注释最多的GOslim的二级分类进行绘图，共计80条目，结果如图6所示，在BP中注释的基因数为3 530，涉及最多基因的条目包括转录调控过程（regulation of transcription，DNA-templated）、跨膜转运（transmembrane transport）、磷酸烯醇式丙酮酸依赖性糖磷酸转移酶系统（phosphoenolpyruvate-dependent sugar phosphotransferase system）、碳水化合物代谢过程（carbohydrate metabolic process），分别有130、73、63、62个；在CC中注释基因数为3 010个，其中与膜的组成部分（integral component of membrane）、质膜（plasma membrane）、细胞质（cytoplasm）相关的基因表现出最高相关性，各有950、677、540个；MF大类中注释的基因数为5 805，其中涉及最多基因的条目为ATP结合（ATP binding）、DNA结合（DNA binding）、金属离子结合（metal ion binding），其数量分别为397、390和325个。
2.4.3　TCDB转运蛋白分类数据库注释
TCDB是对膜转运蛋白进行分类的一个数据库，包括一套转运蛋白分类系统，对目的蛋白质序列进行注释，结果如图7所示，主要注释到7个蛋白家族，共有1 363个基因在TCDB中注释到，分别为primary active transporters（475个基因）、electrochemical potential-driven transporters（321个基因）、channels/pores（211个基因）、incompletely characterized transport systems（176个基因）、group translocators（86个基因）、accessory factors involved in transport（53个基因）、transmembrane electron carriers（40个基因）。
2.4.4　碳水化合物活性酶（CAZy）分析
CAZy是分析碳水化合物酶的基因组、结构和生物化学信息的数据库，使用HMMER基于CAZy数据库对蛋白质序列进行注释，E-value临界值设置为1×10-18，CAZy分析的结果统计如表2所示，在CAZy共注释到97个基因，其中糖苷水解酶GHs注释到的相关基因有42个，糖基转移酶GTs注释到的相关基因有36个，碳水化合物酯酶CEs注释到8个相关基因，辅助氧化还原酶AAs注释到3个相关基因，碳水化合物结合模块CBMs注释到3个相关基因。
2.4.5　PHI分析和T3SS分析结果
在福氏志贺菌Fc株中共有2 052个基因在PHI数据库中得到注释，PHI（Pathogen Host Interactions）是病原与宿主互作数据库，其中，有11个基因突变后毒力减弱，20个突变后致死，69个基因突变后丧失致病性，477个基因突变后不受影响，57个突变成效应子，3个突变后有化学敏感性，另有111个基因突变后可能会增加毒力。
Ⅲ型分泌系统是一种多蛋白复合物，在于革兰阴性病原菌中，负责转运毒力因子到宿主细胞中。使用软件EffectiveT3预测Ⅲ型分泌系统效应蛋白，在T3SS分析中，注释得到福氏志贺菌含有495个T3SS效应蛋白。
2.5　毒力和耐药性基因注释分析
2.5.1　毒力基因注释
对VFDB最新数据库进行注释，经BLAST比对，选取E value≤1×10-5的结果如表3所示，在福氏志贺菌Fc株基因组中共检测到了1 410个潜在的毒力基因，包括介导黏附、侵入、铁摄取以及抗吞噬能力的蛋白。其中注释到的毒力因子类别主要在效应子传递系统（effector delivery system）包括182个基因、营养/代谢因素（nutritional/metabolic factor）包括385个基因、运动性（motility）包括105个基因、免疫调节（immune modulation）包括238个基因、顺从性（adherence）包括239个基因。其中在这些类别中荚膜（capsule）和周毛鞭毛（peritrichous flagella）相关基因最多，分别为68和59个基因。
2.5.2　抗生素耐药性（CARD）分析结果
通过综合抗生素耐药性（Comprehensive Antibiotic Resistance Database，CARD）数据库注释分析，发现福氏志贺菌Fc株有80个耐药基因在数据库中得到注释，结果如表4所示。有关抗生素外排泵的耐药基因有45个，有关抗生素失活的耐药基因有17个，有关抗生素靶标改变的耐药基因有14个，有关抗生素靶标保护的耐药基因有2个，有关抗生素靶标替换的耐药基因有2个。其中对氟喹诺酮类产生耐药的基因主要有gadX、gadW、mdtF、mdtE、AcrF、acrE、mdtH、tolC、marA等，对复合磺胺类产生耐药的基因有sul3，对头孢菌素类抗生素产生耐药的基因的主要有KpnE、marA、acrB和TEM-1等。对β-内酰胺类耐药的基因有blaCXT-M-55。结果表明本研究中福氏志贺菌Fc株携带多种耐药基因，可能是介导其对多种药物耐药的重要原因之一。
2.6　系统进化分析
构建分离株福氏志贺菌Fc株的16S rRNA基因系统进化树，通过将测序结果在NCBI上比对，结果如图8所示，该菌与登录号为NR 026331.1福氏志贺菌相似性高达99%，因此该菌为福氏志贺菌。选取20株与该菌相似性较高的菌构建进化树，菌株福氏志贺菌Fc株与福氏志贺菌ATCC 29903属于同一分支，进化关系最近，与Escherichia albertii strain NBRC 102203进化关系较近，同其他等菌株的进化关系较远。
3　讨论
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志贺菌引起的细菌性痢疾通过消化道传播后在人群中引起普遍感染，不同菌群及血清型间无交叉保护性免疫，并且容易反复感染并出现并发症［21］，临床表现主要为血性腹泻、腹痛和发热等，近几十年时间内，细菌性痢疾死亡率出现明显下降的趋势，但每年仍有约16.4万人死于细菌性痢疾［22］。目前对于志贺菌还没有许可疫苗，因此抗生素治疗是有效手段，可缓解患者病情和降低菌痢传播的风险。目前我国仍是世界上最大的抗生素使用国之一，由于志贺菌可以通过质粒、整合子等可移动元件，从其他细菌中获得耐药基因，导致志贺菌的耐药性不断增加。福氏志贺菌Fc株，全基因组大小为4.98 Mb，GC的平均含量为50.76%，编码基因的总长度为5 006 971 bp，编码的基因为5 750个，平均长度为871 bp，编码基因总长度占全基因的88.63%。Fc株有5 350个基因在NR数据库中得到注释，其中被注释到具有生物活性的蛋白质编码基因共4 934个。
目前基于表型对志贺菌分型的方法主要包括形态特征、血清分型、生化分型和噬菌体分型等，常用于细菌溯源的技术有DNA指纹图谱技术和DNA测序技术［23］。在《方案（2023年版）》报告中指出，对于细菌性痢疾的确诊，基于粪便培养或核酸检测呈阳性［24］。对于临床细菌性痢疾的诊断，基于流行病学史、细菌性痢疾的典型表现和相应的粪便镜检结果为判断标准。
治疗菌痢常用抗生素包括喹诺酮类、复合磺胺类和头孢类药物［25］。然而临床上抗生素的滥用会导致志贺菌出现多重耐药的情况。本研究分离出福氏志贺菌为多重耐药菌株，对头孢菌素类、喹诺酮类、四环素类和β-内酰胺类抗生素的耐药性逐渐增高，检测出80种耐药基因，包括编码16种不同抗生素的基因，与吴自豪等［26］从牛羊粪源中检出的志贺菌耐药情况类似，包括β-内酰胺类、大环内酯类、氨基糖苷类、四环素类、多肽类、酰胺醇类、磺胺类、利福霉素类和林可霉素类。福氏志贺菌的药敏结果也解释了牛腹泻病对多种抗生素治疗没有治疗作用的原因，携带对氟喹诺酮类耐药的基因包括：gadX、gadW、mdtF、mdtE、AcrF、acrE、mdtH、tolC和marA；携带sul3对复合磺胺类产生耐药，携带KpnE、marA、acrB和TEM-1对头孢菌素类抗生素耐药。我国作为养牛大国存栏量位居全球第三，而在肉牛养殖中犊牛期是饲养中最重要的环节之一，犊牛腹泻是一种常见的消化道疾病，也是断奶前犊牛死亡的主要原因之一［27］，是养牛业产业中造成最大经济损失的疾病之一，其中细菌性感染通常可造成急性腹泻，且牛群中传播速度极快［28］。
4　结论
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本研究通过细菌学分离和血清型特异性引物PCR鉴定的方法，从牛粪便中分离鉴定出一株福氏志贺菌Fc株，GO注释分析显示，转录调控过程、跨膜转运、磷酸烯醇式丙酮酸依赖性糖磷酸转移酶系统和碳水化合物代谢过程是基因富集程度最高的途径；KEGG分析中基因富集最高的代谢途径分别为膜传输和氨基酸代谢；TCDB转运蛋白分析显示，有7个蛋白家族共1 363个基因在TCDB数据库中注释到；CAZy注释分析有97个基因为碳水化合物酶，PHI分析显示有2 052个基因在III型分泌系统中得到注释，部分基因的突变会影响细菌的毒力和致病性；CARD注释分析发现80个抗性基因；VFDB注释分析发现1 410个潜在的毒力因子相关基因。系统进化树分析发现福氏志贺菌与福氏志贺菌29903属于同一分支，进化关系最近。本研究完成了一株牛源福氏志贺菌的分离鉴定和全基因组测序分析，对其耐药性进行研究，解析了临床上引起牛腹泻的病原菌的转运蛋白、毒力因子、抗药性以及碳水化合物酶等，推测相关的基因及蛋白家族与福氏志贺菌在临床上致病性有关，为志贺氏菌病的防控研究和用药治疗提供了理论依据。

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doi: 10.11843/j.issn.0366-6964.2026.01.033
  • 接收时间：2025-01-09
  • 首发时间：2026-09-16
  • 出版时间：2026-01-23
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  • 收稿日期：2025-01-09
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    北京农学院动物科学技术学院，兽医学（中兽医）北京市重点实验室，北京 102206

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王真，主要从事动物疫病防控技术、细菌致病及耐药机制研究，E-mail：
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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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