Comparative pathological study of tilapia naturally infected with Streptococcus agalactiae and virulence gene profiling of isolated strains
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摘要:
在自然感染无乳链球菌(Streptococcus agalactiae)的罗非鱼(Oreochromis niloticus)成鱼、稚鱼和自然携带无乳链球菌的罗非鱼体内分别获得14株、4株和2株无乳链球菌。临床和组织病理学分析显示，罗非鱼成鱼出现无规则游动，脑、眼眶、鳃和鳍条充血，眼球突出、白浊，内脏器官肿大、充血，以肾小管玻璃样变性、脑膜炎和心外膜炎等组织病理学变化为特征；罗非鱼稚鱼体表无明显症状，但部分内脏器官呈现肿大、充血现象，以脾脏血管区出血、肾小管上皮细胞变性、脑组织炎症反应较轻为其主要组织病理学特征。此外，罗非鱼胃固有层内及稚鱼肝脏组织中有大量的嗜酸性粒细胞浸润，可观察到无乳链球菌在成鱼的脑、心脏以及稚鱼肝脏中增殖；自然携带无乳链球菌的罗非鱼临床症状和组织学病变均不明显。PCR检测发现，各无乳链球菌毒力基因谱相同，但自然感染无乳链球菌的罗非鱼成鱼、稚鱼和自然携带无乳链球菌的罗非鱼的病理学损伤差异显著。
Abstract:We isolated 14, 4 and 2 strains of Streptococcus agalactiae from naturally infected adult and juvenile tilapia as well as tilapia naturally carrying S. agalactiae, respectively. The clinical signs and anatomy changes of adult tilapia were as follows: erratic swimming, congestion of brain, eyeballs, gills and fins, exophthalmia, corneal opacity and swelling of visceral organs, which were characterized by histopathological changes with tubular hyaline degeneration, meningitis and epicarditis. The clinical symptoms of juvenile tilapia were not obvious, but some of the internal organs showed swelling and congestion, characterized by main histopathological features of hemorrhage of spleen vascular area, degenerated renal tubular epithelial cells and milder inflammatory response in brain tissue. In addition, eosinophil infiltration was found in the lamina propria of tilapia and in the liver of juvenile fish. It was observed that S. agalactiae proliferated in the brain and heart of adult fish and in the liver of juvenile tilapia, respectively. The clinical symptoms and histological lesions in tilapia carrying S. agalactiae were not obvious. The results of PCR detection show that all the S. agalactiae strains had the same virulence gene profiles, but there were significant differences in pathological damages among adult fish, juvenile fish and tilapia carrying S. agalactiae.
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图 1 罗非鱼脑组织PCR检测结果
M. Maker DL 2 000；阳. 阳性对照；阴. 阴性对照；1~159. 采自开平养殖场；160~166. 采自高州平养殖场；167~170. 采自廉江养殖场；171~174. 采自吴川养殖场；175~180. 采自惠州养殖场；181~188. 采自河源养殖场
Figure 1. PCR detection results of tilapia brain
positive. positive control; negative. negative control; 1−159. from Kaiping farm; 160-166. from Gaozhouping farm; 167−170. from Lianjiang farm; 171−174. from Wuchuan farm; 175−180. from Huizhou farm; 181−188. from Heyuan farm
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图 2 鱼感染无乳链球菌的眼观剖检变化
罗非鱼成鱼：A. 眼眶充血、眼球突出(↓)，肠道发炎、肠壁变薄、内容物发黄(*)；B. 脑充血、出血(↓)；C. 肝脏肿大、充血、胆囊肿大(*)，脾脏肿大、充血，肾脏肿大(↓)。罗非鱼稚鱼：体表无明显症状；D. 肝脏充血肿大(*)，脾脏肿大(*)，肠壁变薄、内容物发黄；自然携带无乳链球菌罗非鱼：E. 体表正常；内脏无明显症状。斑马鱼：F. 身体弯曲，眼球浑浊，鳍条和腹部充血、出血(↓)
Figure 2. Change in anatomy of fish infected with S. agalactiae
Adult tilapia: A. orbital congestion and exophthalmos (↓), intestinal inflammation, thinning of intestinal wall and yellowing of contents (*); B. cerebral hyperemia and hemorrhage (↓); C. liver enlargement, congestion, gallbladder enlargement (*), splenomegaly, hyperemia and kidney enlargement (↓). Juvenile tilapia: no obvious symptoms on the body surface; D. hepatic hyperemia (*), splenomegaly (*), thinning of intestinal wall and yellowing of contents; tilapia naturally carrying S. agalactiae: E. no obvious symptoms on the body surface; no visceral symptoms. Zebrafish: F. bent body, corneal opacity, and congestion of fins (↓)
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图 3 各株无乳链球菌感染斑马鱼后的累积死亡率
Figure 3. Cumulative motality rate of zebrafish infected with different S. agalactiae strains
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图 4 自然感染无乳链球菌罗非鱼成鱼组织病理学
A. 脑，脑膜炎，脑膜增厚，大量的炎症细胞浸润，脑血管充血；B. 脑，A图
Figure 4. Histopathology of adult tilapia naturally infected with S. agalactiae
A. brain, meningitis, thickening of the meninges, infiltration of a large number of inflammatory cells, cerebral vascular congestion; B. brain,magnified micrograph of the zone in the black frame in A, inflammatory cell aggregation (*), a large number of proliferating S. agalactiae around the blood vessels (↓); C. brain, intravascular microthrombus formation (↓); D. liver, focal inflammatory response, massive accumulation of inflammatory cells (*); E. intestinal, lamina propria congestion (↓), epithelial cells slightly shed; F. gill, gill filament epithelial cell hyperplasia, fusion (↓), sinus congestion (*); G. heart, epicarditis, epicardial thickening, a large number of inflammatory cell infiltration; H. heart, magnified micrograph of the zone in the black frame in G, massive proliferation around the blood vessels S. agalactiae (↓), intravascular inflammatory cell proliferation (*); I. heart, epicardial septic foci, a large number of cells, cell debris (*) and neutrophils in the abscess (↓); J. spleen , hemorrhage (*), splenic artery epithelial cell damage, thrombosis (↓); K. stomach, gastric lamina propria inflammation, vascular congestion (*), a large number of eosinophil infiltration in the inflammation area (↓); L. kidney, kidney tubulous degeneration (↓), renal interstitial hemorrhage (*)
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图 5 自然感染无乳链球菌罗非鱼稚鱼组织病理学
A. 脑，脑炎，小胶质细胞聚集，血管充血；B. 脑，A图
Figure 5. Histopathology of juvenile tilapia naturally infected with S. agalactiae
A. brain, encephalitis, microglia accumulation, vascular congestion; B. brain, magnified micrograph of the zone in the black frame in A, massive proliferation of microglia (*) and vascular congestion (↓); C. liver, liver hemorrhage (*), blood vessels a large number of eosinophil infiltration around; D. liver, magnified micrograph of the zone in the black frame in C, large proliferation of S. agalactiae (*) and hyperplastic eosinophils (↓); E. intestinal, intestinal villi shortened (↓), epithelial cell shedding (*); F. gill, gill silk epithelial cell shedding is "sticky"(↓), sinus congestion (*); G. heart; H. spleen, lymphocyte area shrinkage, vascular area bleeding (*); I. stomach, Inflammatory reaction in the lamina propria of the stomach; J. stomach, magnified micrograph of the zone in the black frame in I, a large number of eosinophils (↓) and neutrophil accumulation (*); K. kidney, tubular degeneration, necrosis; L. kidney, magnified micrograph of the zone in the black frame in K, renal tubular epithelial cells degeneration, shedding (*)
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图 6 自然携带无乳链球菌的罗非鱼组织病理学
A. 脑；B. 肝脏，肝细胞轻微肿胀；C. 肠道；D. 鳃；E. 心脏；F. 脾脏，脾血窦充血；G. 胃，固有层轻微水肿；H. 肾脏，肾小管上皮轻微变性
Figure 6. Histopathology of tilapia carrying S. agalactiae
A. brain; B. liver, liver cells slightly swollen; C. intestine; D. gill; E. heart; F. spleen, spleen sinus congestion; G. stomach, lamina propria edema; H. kidney, the epithelium of kidney tubules is slightly degenerated.
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图 7 无乳链球菌21种毒力基因PCR扩增
M. DNA Marker (DL 2 000); 1. TKP1601; 2. TGZ1601
Figure 7. PCR amplification of 21 virulence gene of S. agalactiae
表 1 样品采集和无乳链球菌菌株分离信息
Table 1 Sample collection and information of separation of S. agalactiae strain
质量/g
mass采样地
sampling city养殖密度/尾·hm–2
breeding density/ind·hm–2发病史
history of disease样品数/尾
number of samples菌株数
number of strains菌株编号
strain No.检出率/%
detection rate≈500 开平市 ≈100 无 159 2 TKP1601-02 1.26 ≈15 高州市 ≈200 爆发 7 4 TGZ1601-04 57.10 ≈500 廉江市 4 4 TLJ1601-04 63.64 吴川市 4 2 TWC1601-02 惠州市 6 0 − 河源市 8 8 TLC1601-08 
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表 2 引物列表
Table 2 Primers of this study
引物
primer上游引物序列 (5'−3')
forward primer sequence下游引物序列 (5'−3')
reverse primer sequence扩增靶标
amplification target长度/bp
length16S rDNA-F/R AGAGTTTGATCC TGGCTCAG TACGGCTACCTTGTTACGACTT 16S rDNA 1 472 sdi-F/R ATTCTCCTCCTGGCAAAGCC TGACGCTTGGTAGTTGCTGT 16S−23S rDNA 192 fbsA-F/R AGTGTTGGAAATCAAAGTCAAGGT TTCATTGCGTCTCAAACCGC 纤维蛋白结合蛋白A (fbsA) 924 cfb-F/R AACTCTAGTGGCTGGTGCAT CTCCAACAGCATGTGTGATTGC CAMP因子基因 (cfb) 650 dltR-F/R GTCTGAAGGTCCCCAAACCT TGTTACCCAAACGCTCAGGAT 调节蛋白基因 (dltR) 392 ponA-F/R ACAACTTGCTTTGCTCGCTG AGAGCCCTTCTGGCATTGTC 青霉素结合蛋白基因 (ponA) 1 337 hylB-F/R TCCACAACCCGTCACAACAC AACGCGCCCCATATCTACTA 透明质酸酶基因 (hylB) 790 cspA-F/R TGCACGTAACCAGTATCGCA GCACCGAGTTTAACGGCATC 丝氨酸蛋白酶基因 (cspA) 175 sodA-F/R TGATGCGCTTGAGCCACATA GCTTTGATGTAGTTAGGACGAACA 超氧化物歧化酶基因 (sodA) 513 sip-F/R ACAGATACGACGTGGACAGC ACCACGATCTGGCATTGCAT 表面免疫相关蛋白基因 (sip) 1 173 fbsB-F/R AGTTGCGCAAACTTCTGTCC TTTCCGCAGTTGTTACACCG 纤维蛋白结合蛋白B基因 (fbsB) 158 iagA-F/R GCATGGCCATTCCACTGAAG GCTAGCACTCATGGCACCTT 侵袭相关基因 (iagA) 493 scpB-F/R TGCGGCCTTTATCAGTCGAA AACAGTCCCATGATACCCGC C5a肽酶基因 (scpB) 273 bca-F/R TCAAGTTTGGTGCAGCTTCTG TCCGGTACTGACAATACTAACAAT αC蛋白基因 (bca) 616 srr-1-F/R ATGTTGCAGTAAAGCGCTGC GGAAGAGAGTCGTTTTCGGC 富含丝氨酸重复蛋白基因 (srr-1) 727 bibA-F/R TGCATAATATCCAGGTGTAGGCA TGAGAGATTGGGAAGTGGTGC 免疫原性细菌黏附蛋白基因 (bibA) 943 psaA-F/R AGCTGTCACCCTTTTGACCTT TAGGCTTAGGTGCCTGTGCT 肺炎球菌表面抗原A基因 (psaA) 828 lmb-F/R ATTTGTGACGCAACACACGG TCTTGTTTCCGCTTGGAGCA 层黏连蛋白结合蛋白基因 (lmb) 263 spb1-F/R GACATGGGGAGATGGTGGTG AGCTTCTGTGCCCCATTCAA 溶血素Ⅲ (spb1) 652 bac-F/R TGATTCCCTTTTGCTCTGCCA GTTCATGGGAAGCGTTGCTC βC蛋白基因 (bac) 557 pavA-F/R TCGACTTACATTGCCCCACC GGCGGCATCTGTCTTAACCT 纤维蛋白结合蛋白基因 (pavA) 996 cppA-F/R TGCAAATCTTGTCCCTGTGC TCGTACTCGTGCGGTGAATG C3降解蛋白酶基因 (cppA) 387 cylE-F/R ATTCTCCTCCTGGCAAAGCC TGACGCTTGGTAGTTGCTGT β-溶血素/溶细胞素基因 (cylE) 176
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表 3 21对毒力基因检测结果
Table 3 Detection results of 21 virulence genes
毒力基因
virulence gene菌株 strain 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 fbsA + + + + + + + + + + + + + + + + + + + + cfb + + + + + + + + + + + + + + + + + + + + dltR + + + + + + + + + + + + + + + + + + + + ponA + + + + + + + + + + + + + + + + + + + + hylB + + + + + + + + + + + + + + + + + + + + cspA + + + + + + + + + + + + + + + + + + + + sodA + + + + + + + + + + + + + + + + + + + + sip + + + + + + + + + + + + + + + + + + + + fbsB + + + + + + + + + + + + + + + + + + + + iagA + + + + + + + + + + + + + + + + + + + + scpB – – – – – – – – – – – – – – – – – – – – bca + + + + + + + + + + + + + + + + + + + + srr-1 + + + + + + + + + + + + + + + + + + + + bibA + + + + + + + + + + + + + + + + + + + + psaA + + + + + + + + + + + + + + + + + + + + lmb – – – – – – – – – – – – – – – – – – – – spb1 + + + + + + + + + + + + + + + + + + + + bac + + + + + + + + + + + + + + + + + + + + pavA + + + + + + + + + + + + + + + + + + + + cppA + + + + + + + + + + + + + + + + + + + + cylE + + + + + + + + + + + + + + + + + + + + 注：1−2. TKP1601−TKP1602；3−6. TGZ1601−TGZ1604；7−10. TLJ1601−TLJ1604；11−12. TWC1601−TWC1602；13−20. TLC1601−
TLC1608
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[1] 顾慧敏, 胡引. 1例分娩期合并无乳链球菌败血症患者的抢救及护理[J]. 中国实用护理杂志, 2014, 30(12): 56-57. [2] SANZROJAS P, CABEZAOSORIO L, HERMOSA C, et al. Acute meningitis by Streptococcus agalactiae in a immunocompetent male[J]. Rev Esp Quim, 2013, 26(1): 78-79.
[3] JAWA G, HUSSAIN Z, da SILVA O. Recurrent late-onset group B Streptococcus sepsis in a preterm infant acquired by expressed breastmilk transmission: a case report[J]. Breastfeed Med, 2013, 8(1): 134-136. doi: 10.1089/bfm.2012.0016
[4] VILLENA R M A, OLALLA S J, de la TORRE L J, et al. Streptococcus agalactiae induced cavitated pneumonia[J]. Rev Clin Esp, 2009, 209(5): 252-254. doi: 10.1016/S0014-2565(09)71245-7
[5] ELLIOTT J A, FACKLAM R R, RICHTER C B. Whole-cell protein patterns of nonhemolytic group B, type Ib, streptococci isolated from humans, mice, cattle, frogs, and fish[J]. J Clin Microbiol, 1990, 28(3): 628-630.
[6] EVANS J J, BOHNSACK J F, KLESIUS P H, et al. Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan[J]. J Med Microbiol, 2008, 57(11): 1369-1376. doi: 10.1099/jmm.0.47815-0
[7] GENG Y, WANG K Y, HUANG X L, et al. Streptococcus agalactiae, an emerging pathogen for cultured ya-fish, Schizothorax prenanti, in China[J]. Transbound Emerg Dis, 2012, 59(4): 369-375. doi: 10.1111/tbed.2012.59.issue-4
[8] 崔静雯, 汪开毓, 贺扬, 等. 无乳链球菌感染尼罗罗非鱼的脑膜炎模型[J]. 水产学报, 2015, 39(12): 1883-1893. [9] 王瑞, 李莉萍, 黄婷, 等. 罗非鱼组织内无乳链球菌实时荧光定量PCR检测方法建立[J]. 南方水产科学, 2015, 11(3): 41-46. doi: 10.3969/j.issn.2095-0780.2015.03.007 [10] 卢迈新, 黎炯, 叶星, 等. 广东与海南养殖罗非鱼无乳链球菌的分离、鉴定与特性分析[J]. 微生物学通报, 2010, 37(5): 766-774. [11] HEMÁNDEZ E, FIGUEROA J, IREGUI C. Streptococcosis on a red tilapia, Oreochromis sp., farm: a case study[J]. J Fish Dis, 2009, 32(3): 247-252. doi: 10.1111/jfd.2009.32.issue-3
[12] 祝璟琳, 杨弘. 鱼源无乳链球菌致病机理研究进展[J]. 广东海洋大学学报, 2013, 33(6): 92-96. [13] CHIDEROLI R T, AMOROSO N, MAINARDI R M, et al. Emergence of a new multidrug-resistant and highly virulent serotype of Streptococcus agalactiae in fish farms from Brazil[J]. Aquaculture, 2017, 479: 45-51. doi: 10.1016/j.aquaculture.2017.05.013
[14] 韦现色, 林勇, 杨慧赞, 等. 广西罗非鱼链球菌病的流行及防治[J]. 广西畜牧兽医, 2013, 29(1): 57-60. doi: 10.3969/j.issn.1002-5235.2013.01.031 [15] 方伟, 梁宇恒, 宁丹, 等. 广东地区感染养殖罗非鱼的无乳链球菌分子分型研究[J]. 中山大学学报(自然科学版), 2016, 55(2): 97-101. [16] SU Y L, FENG J, LIU C, et al. Dynamic bacterial colonization and microscopic lesions in multiple organs of tilapia infected with low and high pathogenic Streptococcus agalactiae strains[J]. Aquaculture, 2017, 471: 190-203. doi: 10.1016/j.aquaculture.2017.01.013
[17] PATRAS K A, NIZET V. Group B streptococcal maternal colonization and neonatal disease: molecular mechanisms and preventative approaches[J]. Front Pediatr, 2018, 6: 27. doi: 10.3389/fped.2018.00027
[18] LECLERCQ S Y, SULLIVAN M J, IPE D S, et al. Pathogenesis of Streptococcus urinary tract infection depends on bacterial strain and β-hemolysin/cytolysin that mediates cytotoxicity, cytokine synthesis, inflammation and virulence[J]. Sci Rep-UK, 2016, 6: 29000. doi: 10.1038/srep29000
[19] GENDRIN C, LEMBO A, WHIDBEY C, et al. The sensor histidine kinase RgfC affects group B streptococcal virulence factor expression independent of its response regulator RgfA[J]. Infect Immun, 2015, 83(3): 1078-1088. doi: 10.1128/IAI.02738-14
[20] 李庆勇, 可小丽, 卢迈新, 等. 罗非鱼无乳链球菌C5a肽酶(ScpB)的原核表达及其免疫原性[J]. 中国水产科学, 2014, 21(1): 169-179. [21] 曾祖聪, 可小丽, 卢迈新, 等. 罗非鱼无乳链球菌LrrG-Sip融合蛋白免疫原性研究[J]. 南方水产科学, 2017, 13(3): 51-57. doi: 10.3969/j.issn.2095-0780.2017.03.007 [22] ZHANG D, LI A, GUO Y, et al. Molecular characterization of Streptococcus agalactiae in diseased farmed tilapia in China[J]. Aquaculture, 2013, 412(6): 64-69.
[23] KANNIKA K, PISUTTHARACHAI D, SRISAPOOME P, et al. Molecular serotyping, virulence gene profiling and pathogenicity of Streptococcus agalactiae isolated from tilapia farms in Thailand by multiplex PCR[J]. J Appl Microbiol, 2017, 122(6): 1497-1507. doi: 10.1111/jam.2017.122.issue-6
[24] BERRIDGE B R, BERCOVIER H, FRELIER P F. Streptococcus agalactiae and Streptococcus difficile 16S-23S intergenic rDNA: genetic homogeneity and species-specific PCR[J]. Vet Microbiol, 2001, 78(2): 165-173. doi: 10.1016/S0378-1135(00)00285-6
[25] PATTERSON H, SARALAHTI A, PARIKKA M, et al. Adult zebrafish model of bacterial meningitis in Streptococcus agalactiae infection[J]. Dev Comp Immunol, 2012, 38(3): 447-455. doi: 10.1016/j.dci.2012.07.007
[26] KAYANSAMRUAJ P, PIRARAT N, KATAGIRI T, et al. Molecular characterization and virulence gene profiling of pathogenic Streptococcus agalactiae populations from tilapia (Oreochromis sp.) farms in Thailand[J]. J Vet Diagn Invest, 2014, 26(4): 488. doi: 10.1177/1040638714534237
[27] GODOY D T, CARVALHOCASTRO G A, LEAL C A, et al. Genetic diversity and new genotyping scheme for fish pathogenic Streptococcus agalactiae[J]. Lett Appl Microbiol, 2013, 57(6): 476-483. doi: 10.1111/lam.2013.57.issue-6
[28] UDO E E, BOSWIHI S S, ALSWEIH N. Genotypes and virulence genes in group B Streptococcus isolated in the maternity hospital, Kuwait[J]. Med Prin Pract, 2013, 22(5): 453-457. doi: 10.1159/000349932
[29] RAJAGOPAL L. Understanding the regulation of group B streptococcal virulence factors[J]. Future Microbiol, 2009, 4(2): 201-221. doi: 10.2217/17460913.4.2.201
[30] EVANS J J, PASNIK D J, KLESIUS P H. Differential pathogenicity of five Streptococcus agalactiae isolates of diverse geographic origin in Nile tilapia (Oreochromis niloticus L.)[J]. Aquacult Res, 2015, 46(10): 2374-2381. doi: 10.1111/are.2015.46.issue-10
[31] 祝璟琳, 邹芝英, 李大宇, 等. 尼罗罗非鱼无乳链球菌病的病理学研究[J]. 水产学报, 2014, 38(11): 1937-1944. [32] ABUSELIANA A F, DAUD H H M, AZIZ S A, et al. Pathogenicity of Streptococcus agalactiae isolated from a fish farm in selangor to juvenile red tilapia (Oreochromis sp.)[J]. J Anim Vet Adv, 2011, 10(7): 914-919. doi: 10.3923/javaa.2011.914.919
[33] 姜建强, 额尔敦木图, 包花尔, 等. 嗜酸性粒细胞与寄生虫感染免疫的相关性[J]. 黑龙江畜牧兽医, 2016(2): 63-67. [34] REIMERT C M, FITZSIMMONS C M, JOSEPH S, et al. Eosinophil activity in Schistosoma mansoni infections in vivo and in vitro in relation to plasma cytokine profile pre- and posttreatment with praziquantel[J]. Clin Vaccine Immunol, 2006, 13(5): 584-593. doi: 10.1128/CVI.13.5.584-593.2006
[35] DORAN K S, LIU G Y, NIZET V. Group B streptococcal β-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis[J]. J Clin Invest, 2003, 112(5): 736-744. doi: 10.1172/JCI200317335
[36] RING A, BRAUN J S, POHL J, et al. Group B streptococcal β-hemolysin induces mortality and liver injury in experimental sepsis[J]. J Infect Dis, 2002, 185(12): 1745-1753. doi: 10.1086/jid.2002.185.issue-12
[37] CHENG Q, CARLSON B, PILLAI S, et al. Antibody against surface-bound C5a peptidase is opsonic and initiates macrophage killing of group B Streptococci[J]. Infect Immun, 2001, 69(4): 2302-2308. doi: 10.1128/IAI.69.4.2302-2308.2001
[38] BOHNSACK J F, WIDJAJA K, GHAZIZADEH S, et al. A role for C5 and C5a-ase in the acute neutrophil response to group B streptococcal infections[J]. J Infect Dis, 1997, 175(4): 847-855. doi: 10.1086/jid.1997.175.issue-4
[39] 胡会杰, 张琪, 周明旭, 等. 不同禽源致病性大肠杆菌毒力基因分布规律研究[J]. 中国家禽, 2015, 37(10): 34-37. [40] LIN P Y, LAN R, SINTCHENKO V, et al. Computational bacterial genome-wide analysis of phylogenetic profiles reveals potential virulence genes of Streptococcus agalactiae[J]. PloS One, 2011, 6(4): e17964. doi: 10.1371/journal.pone.0017964
[41] WANG Z, GUO C, XU Y, et al. Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression[J]. Infect Immun, 2014, 82(6): 2615. doi: 10.1128/IAI.00022-14
[42] BACHRACH G, ZLOTKIN A, HURVITZ A, et al. Recovery of Streptococcus iniae from diseased fish previously vaccinated with a Streptococcus vaccine[J]. Appl Environ Micro, 2001, 67(8): 3756. doi: 10.1128/AEM.67.8.3756-3758.2001
[43] ALHARBI A H. Phenotypic and genotypic characterization of Streptococcus agalactiae isolated from hybrid tilapia (Oreochromis niloticus×O. aureus)[J]. Aquaculture, 2016, 464: 515-520. doi: 10.1016/j.aquaculture.2016.07.036
[44] ELDAR A, BEJERANO Y, LIVOFF A, et al. Experimental streptococcal meningo-encephalitis in cultured fish[J]. Vet Microbiol, 1995, 43(1): 33-40. doi: 10.1016/0378-1135(94)00052-X
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