格林—巴利综合征相关空肠弯曲菌遗传特征分析
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摘要
空肠弯曲菌(Campylobacter jejuni,C.jejuni)是引起肠道感染的主要病原菌之一。除肠炎外,格林—巴利综合征(Guillain-Barre Syndrome,GBS)是空肠弯曲菌感染后的主要继发病症之一,导致GBS的空肠弯曲菌具有特异的遗传特征。2007年6月～7月,我国吉林省长春市发生36人的GBS暴发,流行病学调查结果表明,此次GBS的暴发与近期腹泻的流行密切相关,血清学检测结果显示,空肠弯曲菌是感染的主要病因。为进一步了解我国空肠弯曲菌菌株以及GBS相关菌株的遗传特征,本研究对长春GBS暴发相关菌株、我国河北省GBS患者分离菌株、北方地区腹泻病人、家禽及食物分离菌株进行分型分析,并对暴发GBS患者分离株ICDC07001进行全基因组序列分析。
分析结果发现,长春GBS暴发相关菌株中,7株为空肠弯曲菌,7株为结肠弯曲菌,GBS患者及同期腹泻病人分离的菌株均为空肠弯曲菌。GBS患者分离菌株(ICDC07001)及同期腹泻病人分离菌株(ICDC07002,ICDC07003)的血清型均为HS:41,与GBS患者家养家禽分离菌株血清型不同。8株河北GBS患者分离菌株的血清型分别为S:19、HS:37、HS:2和不可分型。我国其它来源菌株的血清型分布分散,没有明显的优势血清型。
PFGE分析结果发现,GBS暴发相关4株人源菌株带型一致,与3株家禽来源菌株不同。聚类分析显示,GBS暴发相关人源菌株与我国河北部分GBS相关菌株的带型相似。与美国PulseNet弯曲菌PFGE数据库中比较发现,本次GBS暴发相关菌株PFGE带型唯一,但与1995年发生在美国路易斯安娜州的一起水污染导致空肠弯曲菌感染暴发的菌株带型高度相似。其它不同来源菌株的PFGE带型分散,没有显著聚集特征。
MLST分析发现,我国49株空肠弯曲菌分为33个ST型,分别属于13个ST序列群。eBURST聚类分析表明,我国菌株没有形成核心ST型。暴发相关人源菌株ST型相同,为本次研究新发现ST型,被命名为ST-2993。与ST-2993仅一个等位基因差异的ST-1672、ST-27和ST-1377共有4株菌,分别来源于GBS患者、菌血症患者及胃肠炎患者。40株GBS相关菌株的ST型SplitsTree聚类分析结果表明,GBS相关菌株没有形成显著的克隆群。
菌株ICDC07001基因组含有一个染色体和一个拷贝的pTet质粒。质粒ICDC07001_pTet(44.1kb)大小与暴发相关菌株81-176的pTet质粒81-176_pTet(45.2kb)相近,含有37个CDSs。与其它测序菌株相比,ICDC07001(1.66Mb)基因组大小与其它人源空肠弯曲菌空肠亚种基因组相似,小于鸡来源菌株RM1221(1.78Mb)和空肠弯曲菌德莱亚种菌株269.97(1.85Mb)基因组。ICDC07001染色体上有一个反向插入一个大小约32kb的整合元素-弯曲菌Mu样噬菌体(Campylobacter Mu-like phage 1,CMLP1)整合元素的插入。与其它空肠弯曲菌相似,菌株ICDC07001染色体上铁吸收相关序列、细菌限制修饰系统相关序列和细菌表面结构相关序列等表现基因多样性。ICDC07001染色体上没有完整的插入因子或者转座子的插入。基因组序列比较发现,菌株ICDC07001与血清型相同的GBS患者分离菌株260.94有98.99%的基因同源。
经比较获得菌株ICDC07001不同于其它测序菌株特异的25个CDSs,其中23个CDSs属于高变异区基因,分别位于插入整合元素CMLP1上、下游,CPS基因簇、LOS基因簇、FM基因簇、氧化磷酸化相关基因和Ⅰ型限制性修饰系统相关基因序列区域内。1个CDS与编码弯曲菌鞭毛分泌毒素FspA2基因同源,1个CDS与编码幽门螺杆菌插入因子IS606转移酶B基因部分同源。
将ICDC07001分别与感染暴发相关菌株、GBS相关菌株以及胃肠炎相关菌株进行分组两两比较,组内共同基因分别进行组间比较分析,获得感染暴发相关共同基因27个、GBS相关共同基因13个(其中9个属于LOS基因簇基因)和胃肠炎相关共同基因18个。
致病相关因子脂寡糖(LOS)、荚膜多糖(CPS)以及鞭毛基因合成修饰(FM)相关基因簇序列比较发现:菌株ICDC07001的CPS仅与血清型相同菌株260.94高度同源,而与其它GBS相关菌株的CPS同源性很低。LOS基因簇在GBS相关菌株中同源性明显高于其它菌株。菌株ICDC07001的FM基因簇与菌株260.94100%同源,而与其它菌株的同源比例明显降低。ICDC07001的LOS外核区基因簇属于类A类LOS,其唾液酸转移酶基因编码双功能唾液酸转移酶,可表达类神经节苷脂抗体GM1、GD1b的抗体,与GBS暴发患者血清中抗GM1、GD1b抗体显著增高一致。比较发现,黏附侵袭相关基因ciaB、cadF、peb1、jlpa、cdt以及双元调控因子相关基因属于种内保守基因。
以16S rRNA,rpoB,fla以及flaA—SVR基因序列的相似性为基础进行菌株的遗传进化关系分析,结果发现:ICDC07001与260.94遗传距离最近,同时与菌株81-176、81116和HB93.13遗传距离相近。
以菌株NCTC11168为模型,本研究建立了空肠弯曲菌蛋白质数据库,通过比较蛋白质组分析获得菌株在37℃/42℃优势表达蛋白并发现空肠弯曲菌毒力相关蛋白PEB1,CadF和CDT在不同温度下的表达没有显著差异。
本研究建立了空肠弯曲菌感染病原的溯源分析手段,通过基因组的比较分析获得了菌株ICDC07001的特异遗传特征及相关致病因子遗传特点。进一步证明空肠弯曲菌的血清型与菌株的CPS基因相关,菌株感染后导致GBS与菌株的LOS基因相关。通过菌株分组比较,获得了空肠弯曲菌感染暴发、GBS相关以及胃肠炎相关共同基因,为空肠弯曲菌致病机制的研究奠定了基础。本研究建立了空肠弯曲菌蛋白质组数据库,37℃/42℃优势表达蛋白的获得为空肠弯曲菌在人类致病机理的研究提供依据。
Campylobacter jejuni(C.jejuni) is a Gram negative microaerophilic bacterium.It is a major cause of human gastroenteritis world-wide.In addition to the burden of disease due to gastroenteritis,C.jejuni infection is highly associated with the development of Guillain-Barre syndrome(GBS),an acute motor paralysis that may result from autoimmune antibodies against C.jejuni antigens.
Genetic population studies play an important role to investigate the bacterial pathogen and explore the epidemiology of Campylobacter infection.It was reported the GBS associated C.jejuni had specific genetic character.From June to July,2007,36 cases of GBS occurred in one district in Changchun,Jilin,China.Epidemiology and serological study results indicated it was associated with preceding C.jejuni infection. In order to obtain the genetic characteristics of the outbreak associated strains and the relatedness to other Chinese strains,serotyping,PFGE and MLST analyses were preceded on C.jejuni strains from.China.
Seven C.jejuni strains and 7 C.coli strains were identified from the GBS outbreak. The isolates from GBS patients and diarrhea neighbors were C.jejuni.Three of four GBS outbreak associated human isolates(ICDC07001,ICDC07002,and ICDC07003) belonged to serotype HS:41 which were different from the serotype of the strains from GBS patients' house feeding poultry.There were totally 9 kinds of serotype among 26 C.jejuni except 9 strains belonged to un-typed ones.
PFGE were performed according to the standard PulseNet PFGE protocol for C.jejuni (http://www.cdc.gov/pulsenet/protocols/campy_protocol.pdf) with SmaI and KpnI digestions.All four human C.jejuni isolates had indistinguishable SmaI and KpnI PFGE profiles and they were different from the PFGE profiles of the chicken isolates. The PFGE profiles of the GBS outbreak strains were unique when compared to 5,284 entries in the PulseNet National Campylobacter database.This PFGE profile of the human C.jejuni isolates from the GBS outbreak were most closely similar to C.jejuni isolates associated with an outbreak in Louisiana in 1995 and was similar to 4 of GBS associated strains from Hebei province,China.The entire four human C.jejuni isolates from GBS outbreak had the same sequence type(ST).This ST was new in the public MLST database and was assigned ST-2993.The chicken isolates from GBS outbreak were ST379 and ST2274 which had been seen previously in the database.There was no any founder ST was identified from Chinese strains by eBURST cluster analysis. SplitsTree analysis indicated the STs from GBS associated strains did not form any colonal complex.Four isolates from the MLST database had similar MLST profiles with ST-2993.There strains were found being associated with GSB and severe system infection.
The genome size of ICDC07001 was similar with other human C.jejuni isolates such as C.jejuni 81-176,NCTC11168 and 81-116 but smaller than the chichen isolate RM1221 and C.jejuni sub.doylei 269.97.There was one C.jejuni integrated element, a Campylobacter Mu-like phage(also termed CMLP1,encoding several proteins with similarity to bacterio-phage Mu and other Mu-like biosynthesis protein) reversely inserted between CDS01122(Cj0723c,putative integral membrane zinc metalloprotease) and CDS01219(Cj0725c,molybdenum cofactor) in ICDC07001. Similar as other C.jejuni genome character,there were variant genes in the regions of surface structure,such as the lipooligosaccharide(LOS) biosynthesis,Polysaccharide capsular(CPS) biosynthesis,flagella modification(FM),and DNA restriction modification(R/M) loci.From genomic comparative study,ICDC07001 were 98.99% similar with C.jejuni strain 260.94 which was isolated from GBS patient in South Africa and had same serotype with ICDC07001.Twenty five CDSs were found specific on ICDC07001 compared to NCTC11168、81-176,RM1221,81-11,269.97and C.curvus_525.92,C.fetus_82-40 and C.hominis_BAA-381,which were located in the CMLP1,CPS,LOS and FM regions.Three specific CDSs were in Oxidative phosphorylation region.ICDC07001 has a specific FspA2 gene and partial of IS606 tnpB located at the upstream of tonB.Comparative analysis was performed by sorting the studied strains into three groups.Twenty-seven genes were specifically common in the C.jejuni infection outbreak associated group.Eighteen genes were common in the gastroenteritis group and thirteen genes were common in the GBS associated group and nine of them belonged to LOS genes.
LOS cluster of ICDC07001 was similar with type ALOS,which was previously reported to associate with GBS.Sialyl-transferase gene from ICDC07001 was cst-Ⅱ(Asn51) which had bothα-2,3 andα-2,8-sialyltransferase activity.It was referred to express the mimic of the GM1 and GD1b gangliosides which was consistent with the serum anti-gangliosides tests results for GBS patients.The CPS of ICDC07001 was only similar with the same serotype strains 260.94.
Neighbors-joining phylogenetic analysis of Campylobacter and other bacteria based on the similarities of 16SrRNA,rpoB and flaA-SVR gene sequences were performed. A good congruence result was obtained between these genes.The most closely related strain to ICDC07001 was strain 260.94.C.jejuni 81-176,81-116 and HB93-13 were also closed related to ICDC07001.A primary proteomic database of sequenced C.jejuni NCTC11168 was set up in this study.Comparative proteomic analysis was performed between 37℃and 42℃culture in vitro with different media.There were the subsets of optimal expression proteins for certain temperature environment.The optimum expressed proteins at 37℃were most related to the stress enhancer and bio-film forming.We did not find any significantly different expression of the PEB1, CadF and CDT between 37℃and 42℃both in BHI and agar media.
In summary,the present study gave us a comprehensive profile of the genetic character of the GBS associated strains and the strains isolated in China.Pathogen tracking study for the GBS outbreak associated strains proved C.jejuni isolates from human were same but different from the poultry ones.The specific genetic character of ICDC07001 was obtained by the genome comparative analysis which gave us clues for further study.In this study,we found CPS but not LPS genes were related to the serotype of C.jejuni.All the studied GBS associated strains had similar LOS.Optimal expressed proteins under different temperature may contribute to host adaptation or the pathogenic specialty of human disease.
分析结果发现,长春GBS暴发相关菌株中,7株为空肠弯曲菌,7株为结肠弯曲菌,GBS患者及同期腹泻病人分离的菌株均为空肠弯曲菌。GBS患者分离菌株(ICDC07001)及同期腹泻病人分离菌株(ICDC07002,ICDC07003)的血清型均为HS:41,与GBS患者家养家禽分离菌株血清型不同。8株河北GBS患者分离菌株的血清型分别为S:19、HS:37、HS:2和不可分型。我国其它来源菌株的血清型分布分散,没有明显的优势血清型。
PFGE分析结果发现,GBS暴发相关4株人源菌株带型一致,与3株家禽来源菌株不同。聚类分析显示,GBS暴发相关人源菌株与我国河北部分GBS相关菌株的带型相似。与美国PulseNet弯曲菌PFGE数据库中比较发现,本次GBS暴发相关菌株PFGE带型唯一,但与1995年发生在美国路易斯安娜州的一起水污染导致空肠弯曲菌感染暴发的菌株带型高度相似。其它不同来源菌株的PFGE带型分散,没有显著聚集特征。
MLST分析发现,我国49株空肠弯曲菌分为33个ST型,分别属于13个ST序列群。eBURST聚类分析表明,我国菌株没有形成核心ST型。暴发相关人源菌株ST型相同,为本次研究新发现ST型,被命名为ST-2993。与ST-2993仅一个等位基因差异的ST-1672、ST-27和ST-1377共有4株菌,分别来源于GBS患者、菌血症患者及胃肠炎患者。40株GBS相关菌株的ST型SplitsTree聚类分析结果表明,GBS相关菌株没有形成显著的克隆群。
菌株ICDC07001基因组含有一个染色体和一个拷贝的pTet质粒。质粒ICDC07001_pTet(44.1kb)大小与暴发相关菌株81-176的pTet质粒81-176_pTet(45.2kb)相近,含有37个CDSs。与其它测序菌株相比,ICDC07001(1.66Mb)基因组大小与其它人源空肠弯曲菌空肠亚种基因组相似,小于鸡来源菌株RM1221(1.78Mb)和空肠弯曲菌德莱亚种菌株269.97(1.85Mb)基因组。ICDC07001染色体上有一个反向插入一个大小约32kb的整合元素-弯曲菌Mu样噬菌体(Campylobacter Mu-like phage 1,CMLP1)整合元素的插入。与其它空肠弯曲菌相似,菌株ICDC07001染色体上铁吸收相关序列、细菌限制修饰系统相关序列和细菌表面结构相关序列等表现基因多样性。ICDC07001染色体上没有完整的插入因子或者转座子的插入。基因组序列比较发现,菌株ICDC07001与血清型相同的GBS患者分离菌株260.94有98.99%的基因同源。
经比较获得菌株ICDC07001不同于其它测序菌株特异的25个CDSs,其中23个CDSs属于高变异区基因,分别位于插入整合元素CMLP1上、下游,CPS基因簇、LOS基因簇、FM基因簇、氧化磷酸化相关基因和Ⅰ型限制性修饰系统相关基因序列区域内。1个CDS与编码弯曲菌鞭毛分泌毒素FspA2基因同源,1个CDS与编码幽门螺杆菌插入因子IS606转移酶B基因部分同源。
将ICDC07001分别与感染暴发相关菌株、GBS相关菌株以及胃肠炎相关菌株进行分组两两比较,组内共同基因分别进行组间比较分析,获得感染暴发相关共同基因27个、GBS相关共同基因13个(其中9个属于LOS基因簇基因)和胃肠炎相关共同基因18个。
致病相关因子脂寡糖(LOS)、荚膜多糖(CPS)以及鞭毛基因合成修饰(FM)相关基因簇序列比较发现:菌株ICDC07001的CPS仅与血清型相同菌株260.94高度同源,而与其它GBS相关菌株的CPS同源性很低。LOS基因簇在GBS相关菌株中同源性明显高于其它菌株。菌株ICDC07001的FM基因簇与菌株260.94100%同源,而与其它菌株的同源比例明显降低。ICDC07001的LOS外核区基因簇属于类A类LOS,其唾液酸转移酶基因编码双功能唾液酸转移酶,可表达类神经节苷脂抗体GM1、GD1b的抗体,与GBS暴发患者血清中抗GM1、GD1b抗体显著增高一致。比较发现,黏附侵袭相关基因ciaB、cadF、peb1、jlpa、cdt以及双元调控因子相关基因属于种内保守基因。
以16S rRNA,rpoB,fla以及flaA—SVR基因序列的相似性为基础进行菌株的遗传进化关系分析,结果发现:ICDC07001与260.94遗传距离最近,同时与菌株81-176、81116和HB93.13遗传距离相近。
以菌株NCTC11168为模型,本研究建立了空肠弯曲菌蛋白质数据库,通过比较蛋白质组分析获得菌株在37℃/42℃优势表达蛋白并发现空肠弯曲菌毒力相关蛋白PEB1,CadF和CDT在不同温度下的表达没有显著差异。
本研究建立了空肠弯曲菌感染病原的溯源分析手段,通过基因组的比较分析获得了菌株ICDC07001的特异遗传特征及相关致病因子遗传特点。进一步证明空肠弯曲菌的血清型与菌株的CPS基因相关,菌株感染后导致GBS与菌株的LOS基因相关。通过菌株分组比较,获得了空肠弯曲菌感染暴发、GBS相关以及胃肠炎相关共同基因,为空肠弯曲菌致病机制的研究奠定了基础。本研究建立了空肠弯曲菌蛋白质组数据库,37℃/42℃优势表达蛋白的获得为空肠弯曲菌在人类致病机理的研究提供依据。
Campylobacter jejuni(C.jejuni) is a Gram negative microaerophilic bacterium.It is a major cause of human gastroenteritis world-wide.In addition to the burden of disease due to gastroenteritis,C.jejuni infection is highly associated with the development of Guillain-Barre syndrome(GBS),an acute motor paralysis that may result from autoimmune antibodies against C.jejuni antigens.
Genetic population studies play an important role to investigate the bacterial pathogen and explore the epidemiology of Campylobacter infection.It was reported the GBS associated C.jejuni had specific genetic character.From June to July,2007,36 cases of GBS occurred in one district in Changchun,Jilin,China.Epidemiology and serological study results indicated it was associated with preceding C.jejuni infection. In order to obtain the genetic characteristics of the outbreak associated strains and the relatedness to other Chinese strains,serotyping,PFGE and MLST analyses were preceded on C.jejuni strains from.China.
Seven C.jejuni strains and 7 C.coli strains were identified from the GBS outbreak. The isolates from GBS patients and diarrhea neighbors were C.jejuni.Three of four GBS outbreak associated human isolates(ICDC07001,ICDC07002,and ICDC07003) belonged to serotype HS:41 which were different from the serotype of the strains from GBS patients' house feeding poultry.There were totally 9 kinds of serotype among 26 C.jejuni except 9 strains belonged to un-typed ones.
PFGE were performed according to the standard PulseNet PFGE protocol for C.jejuni (http://www.cdc.gov/pulsenet/protocols/campy_protocol.pdf) with SmaI and KpnI digestions.All four human C.jejuni isolates had indistinguishable SmaI and KpnI PFGE profiles and they were different from the PFGE profiles of the chicken isolates. The PFGE profiles of the GBS outbreak strains were unique when compared to 5,284 entries in the PulseNet National Campylobacter database.This PFGE profile of the human C.jejuni isolates from the GBS outbreak were most closely similar to C.jejuni isolates associated with an outbreak in Louisiana in 1995 and was similar to 4 of GBS associated strains from Hebei province,China.The entire four human C.jejuni isolates from GBS outbreak had the same sequence type(ST).This ST was new in the public MLST database and was assigned ST-2993.The chicken isolates from GBS outbreak were ST379 and ST2274 which had been seen previously in the database.There was no any founder ST was identified from Chinese strains by eBURST cluster analysis. SplitsTree analysis indicated the STs from GBS associated strains did not form any colonal complex.Four isolates from the MLST database had similar MLST profiles with ST-2993.There strains were found being associated with GSB and severe system infection.
The genome size of ICDC07001 was similar with other human C.jejuni isolates such as C.jejuni 81-176,NCTC11168 and 81-116 but smaller than the chichen isolate RM1221 and C.jejuni sub.doylei 269.97.There was one C.jejuni integrated element, a Campylobacter Mu-like phage(also termed CMLP1,encoding several proteins with similarity to bacterio-phage Mu and other Mu-like biosynthesis protein) reversely inserted between CDS01122(Cj0723c,putative integral membrane zinc metalloprotease) and CDS01219(Cj0725c,molybdenum cofactor) in ICDC07001. Similar as other C.jejuni genome character,there were variant genes in the regions of surface structure,such as the lipooligosaccharide(LOS) biosynthesis,Polysaccharide capsular(CPS) biosynthesis,flagella modification(FM),and DNA restriction modification(R/M) loci.From genomic comparative study,ICDC07001 were 98.99% similar with C.jejuni strain 260.94 which was isolated from GBS patient in South Africa and had same serotype with ICDC07001.Twenty five CDSs were found specific on ICDC07001 compared to NCTC11168、81-176,RM1221,81-11,269.97and C.curvus_525.92,C.fetus_82-40 and C.hominis_BAA-381,which were located in the CMLP1,CPS,LOS and FM regions.Three specific CDSs were in Oxidative phosphorylation region.ICDC07001 has a specific FspA2 gene and partial of IS606 tnpB located at the upstream of tonB.Comparative analysis was performed by sorting the studied strains into three groups.Twenty-seven genes were specifically common in the C.jejuni infection outbreak associated group.Eighteen genes were common in the gastroenteritis group and thirteen genes were common in the GBS associated group and nine of them belonged to LOS genes.
LOS cluster of ICDC07001 was similar with type ALOS,which was previously reported to associate with GBS.Sialyl-transferase gene from ICDC07001 was cst-Ⅱ(Asn51) which had bothα-2,3 andα-2,8-sialyltransferase activity.It was referred to express the mimic of the GM1 and GD1b gangliosides which was consistent with the serum anti-gangliosides tests results for GBS patients.The CPS of ICDC07001 was only similar with the same serotype strains 260.94.
Neighbors-joining phylogenetic analysis of Campylobacter and other bacteria based on the similarities of 16SrRNA,rpoB and flaA-SVR gene sequences were performed. A good congruence result was obtained between these genes.The most closely related strain to ICDC07001 was strain 260.94.C.jejuni 81-176,81-116 and HB93-13 were also closed related to ICDC07001.A primary proteomic database of sequenced C.jejuni NCTC11168 was set up in this study.Comparative proteomic analysis was performed between 37℃and 42℃culture in vitro with different media.There were the subsets of optimal expression proteins for certain temperature environment.The optimum expressed proteins at 37℃were most related to the stress enhancer and bio-film forming.We did not find any significantly different expression of the PEB1, CadF and CDT between 37℃and 42℃both in BHI and agar media.
In summary,the present study gave us a comprehensive profile of the genetic character of the GBS associated strains and the strains isolated in China.Pathogen tracking study for the GBS outbreak associated strains proved C.jejuni isolates from human were same but different from the poultry ones.The specific genetic character of ICDC07001 was obtained by the genome comparative analysis which gave us clues for further study.In this study,we found CPS but not LPS genes were related to the serotype of C.jejuni.All the studied GBS associated strains had similar LOS.Optimal expressed proteins under different temperature may contribute to host adaptation or the pathogenic specialty of human disease.
引文
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11.席胜军,2004年肠道门诊期间其他感染性腹泻病原学监测 实用预防医学,2005,6(12):1354-1355.
12.侯凤伶,申志新,王英豪等 保定市空肠弯曲菌感染情况调查分析 中国卫生检验杂志,2006,6(16):725-726.
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15.张乐海,高志坚 德州市15岁以下格林-巴利综合征病例的临床和流行病学分析 华南预防医学,2006,32(1):51-52.
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