Expressions of capsular polysaccharide synthetic gene of <i>Streptococcus agalactiae</i> isolated from Nile tilapia(<i>Oreochromis niloticus</i>) and their effects on capsular sialic acid content and bacterial pathogenicity

SHI Hongya; DONG Junjian; ZHANG Defeng; SUN Chengfei; TIAN Yuanyuan; LU Maixin; YE Xing

doi:10.11964/jfc.20170110680

Volume 42 Issue 2

Turn off MathJax

Article Contents

Abstract

References

Journal of fisheries of china > 2018 > 42(2): 291-302. > DOI: 10.11964/jfc.20170110680

SHI Hongya, DONG Junjian, ZHANG Defeng, SUN Chengfei, TIAN Yuanyuan, LU Maixin, YE Xing. Expressions of capsular polysaccharide synthetic gene of Streptococcus agalactiae isolated from Nile tilapia(Oreochromis niloticus) and their effects on capsular sialic acid content and bacterial pathogenicity[J]. Journal of fisheries of china, 2018, 42(2): 291-302. DOI: 10.11964/jfc.20170110680

Citation:

Expressions of capsular polysaccharide synthetic gene of Streptococcus agalactiae isolated from Nile tilapia(Oreochromis niloticus) and their effects on capsular sialic acid content and bacterial pathogenicity

1.
Key Laboratory of Tropical & Subtropical Fisheries Resource Application & Cultivation, Ministry of Agriculture; Pearl River Fisheries Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, China
2.
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China

Funds:

Central Public-interest Scientific Institution Basal Research Fund, CAFS (2017HY-ZC06); National Natural Science Foundation of China (NSFC) (31272688); China Agriculture Research System (CARS-46)

More Information

Corresponding author:
YE Xing. E-mail: gzyexing@163.com
Received Date: January 06, 2017
Revised Date: May 14, 2017
Available Online: November 27, 2017
Published Date: January 31, 2018

Graphical Abstract

Abstract

Abstract

In order to understand the expressions of capsular polysaccharide synthetic gene of Streptococcus agalactiae (GBS) isolated from Oreochromis niloticus (Nile tilapia) and their effects on capsular sialic acid content and bacterial pathogenicity, capsular polysaccharide synthetic gene cpsE, cpsK and neuA of GBS from O. niloticus were cloned in the study. The expression levels of these genes at different temperature were detected by qPCR. Capsular sialic acid content was detected by colorimetric method. The mortality rate of O. niloticusinfected with GBS cultured at different temperature was analyzed by artificial challenge test. The results showed that amino acid sequence analysis encoded by cpsE, cpsK and neuA of GBS had conservative enzyme active sites which were essential for the synthesis of capsular polysaccharide. CpsE and NeuA of GBS isolated from O. niloticus shared high homology with those of GBS isolated from human and other fish species (>97%). The identities ofcpsK of GBS isolated from O. niloticus with those of other fish species (serotype Ia and Ib) and human (serotype Ia, Ib and II~IX) were 56%–100% and 27%–100%, respectively. The expression levels ofcpsK and neuA of GBS cultivated at different temperature were consistent with that of capsular sialic acid content. Capsular sialic acid content and the mortality rate of tilapia infected with GBS cultivated at 28 and 34 °C were increased with the rise of temperature. The mortality rate of tilapia after artificial challenge at 22 °C was the lowest though the highest capsular sialic acid content was observed. The research suggested that the expression levels of CpsK and NeuA played an important role in the process of sialylation of capsular polysaccharide. Higher capsular sialic acid content of GBS cultivated at low temperature may provide protection for it to stay in the host. However, the expressions of some important virulence factors besides capsular sialic acid might be necessary for a strong bacteria pathogenicity for GBS cultivated at higher temperature.
- Oreochromis niloticus,
- Streptococcus agalactiae,
- temperature,
- capsular polysaccharide synthetic gene,
- capsular sialic acid,
- pathogenicity

FullText(HTML)

References (39)

References

[1]	Johri A K, Paoletti L C, Glaser P, et al. Group B Streptococcus: global incidence and vaccine development[J]. Nature Reviews Microbiology, 2006, 4(12): 932-942. doi: 10.1038/nrmicro1552
[2]	Amal M N A, Zamri-Saad M. Streptococcosis in tilapia (Oreochromis niloticus): A review[J]. Pertanika Journal of Tropical Agricultural Science, 2011, 34(2): 195-206.
[3]	张德锋, 可小丽, 刘志刚, 等.中国七种水生动物源无乳链球菌的分子特征及其对斑马鱼的致病性[J].水产学报,2017,41(11):1788-1797. Zhang D F, Ke X L, Liu Z G, et al. Molecular characteristics and the pathogenicity to zebrafish of Streptococcus agalactiae strains isolated from seven aquatic animals in China[J].Journal of Fisheries of China, 2017,41(11):1788-1797 (in Chinese).
[4]	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. Lu M X, Li J, Ye X, et al. Identification and characterizations of Streptococcus agalactiae isolated from tilapia cultured in Guangdong and Hainan provinces[J]. Microbiology China, 2010, 37(5): 766-774 (in Chinese).
[5]	张德锋, 刘礼辉, 任燕, 等. 我国罗非鱼源新型无乳链球菌的分离、鉴定及其分子特征[J]. 中国水产科学, 2015, 22(5): 1044-1054. Zhang D F, Liu L H, Ren Y, et al. Isolation, identification, and molecular characteristics of a new geno-type of Streptococcus agalactiae from cultured tilapia in China[J]. Journal of Fishery Sciences of China, 2015, 22(5): 1044-1054 (in Chinese).
[6]	Li L P, Wang R, Liang W W, et al. Rare serotype occurrence and PFGE genotypic diversity of Streptococcus agalactiae isolated from tilapia in China[J]. Veterinary Microbiology, 2013, 167(3-4): 719-724. doi: 10.1016/j.vetmic.2013.09.001
[7]	Ye X, Li J, Lu M X, et al. Identification and molecular typing of Streptococcus agalactiae isolated from pond-cultured tilapia in China[J]. Fisheries Science, 2011, 77(4): 623-632. doi: 10.1007/s12562-011-0365-4
[8]	郭玉娟, 张德锋, 樊海平, 等. 中国南方地区罗非鱼无乳链球菌的分子流行病学研究[J]. 水产学报, 2012, 36(3): 399-406. Guo Y J, Zhang D F, Fan H P, et al. Molecular epidemiology of Streptococcus agalactiae isolated from tilapia in Southern China[J]. Journal of Fisheries of China, 2012, 36(3): 399-406 (in Chinese).
[9]	祝璟琳, 李大宇, 邹芝英, 等. 高温应激下无乳链球菌感染对尼罗罗非鱼血清生化指标和组织病理的影响[J]. 水产学报, 2016, 40(3): 445-456. Zhu J L, Li D Y, Zou Z Y, et al. The impact of high temperature stress on serum biochemical parameters and histopathology of Oreochromis niloticus infected by Streptococcus agalactiae[J]. Journal of Fisheries of China, 2016, 40(3): 445-456 (in Chinese).
[10]	Lecours M P, Fittipaldi N, Takamatsu D, et al. Sialylation of Streptococcus suis serotype 2 is essential for capsule expression but is not responsible for the main capsular epitope[J]. Microbes and Infection, 2012, 14(11): 941-950. doi: 10.1016/j.micinf.2012.03.008
[11]	Chaffin D O, Mentele L M, Rubens C E. Sialylation of group B streptococcal capsular polysaccharide is mediated by cpsK and is required for optimal capsule polymerization and expression[J]. Journal of Bacteriology, 2005, 187(13): 4615-4626. doi: 10.1128/JB.187.13.4615-4626.2005
[12]	Chang Y C, Olson J, Beasley F C, et al. Group B Streptococcus engages an inhibitory Siglec through sialic acid mimicry to blunt innate immune and inflammatory responses in vivo[J]. PLOS Pathogens, 2014, 10(1): e1003846. doi: 10.1371/journal.ppat.1003846
[13]	von Gunten S, Simon H U. Natural anti-Siglec autoantibodies mediate potential immunoregulatory mechanisms: Implications for the clinical use of intravenous immunoglobulins (IVIg)[J]. Autoimmunity Reviews, 2008, 7(6): 453-456. doi: 10.1016/j.autrev.2008.03.015
[14]	Weiman S, Uchiyama S, Lin F Y C, et al. O-Acetylation of sialic acid on Group B Streptococcus inhibits neutrophil suppression and virulence[J]. Biochemical Journal, 2010, 428(2): 163-168. doi: 10.1042/BJ20100232
[15]	Boulnoisl G J, Jann K. Bacterial polysaccharide capsule synthesis, export and evolution of structural diversity[J]. Molecular Microbiology, 1989, 3(12): 1819-1823. doi: 10.1111/mmi.1989.3.issue-12
[16]	Chaffin D O, Beres S B, Yim H H, et al. The serotype of type Ia and III group B streptococci is determined by the polymerase gene within the polycistronic capsule operon[J]. Journal of Bacteriology, 2000, 182(16): 4466-4477. doi: 10.1128/JB.182.16.4466-4477.2000
[17]	Rubens C E, Heggen L M, Haft R F, et al. Identification of cpsD, a gene essential for type III capsule expression in group B streptococci[J]. Molecular Microbiology, 1993, 8(5): 843-855. doi: 10.1111/mmi.1993.8.issue-5
[18]	Schaffner T O, Hinds J, Gould K A, et al. A point mutation in cpsE renders Streptococcus pneumoniae nonencapsulated and enhances its growth, adherence and competence[J]. BMC Microbiology, 2014, 14: 210. doi: 10.1186/s12866-014-0210-x
[19]	Shainheit M G, Valentino M D, Gilmore M S, et al. Mutations in pneumococcal cpsE generated via in vitro serial passaging reveal a potential mechanism of reduced encapsulation utilized by a conjunctival isolate[J]. Journal of Bacteriology, 2015, 197(10): 1781-1791. doi: 10.1128/JB.02602-14
[20]	丁丹丹. 猪链球菌2型cps2E基因缺失株构建及生物学特性研究[D]. 武汉: 华中农业大学, 2014. Ding D D. Construction and characterization of cps2E deleted mutants of Streptococcus Suis Serotype 2[D]. Wuhan: Huazhong Agricultural University, 2014 (in Chinese).
[21]	Lewis A L, Nizet V, Varki A. Discovery and characterization of sialic acid O-acetylation in group B Streptococcus[J]. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(30): 11123-11128. doi: 10.1073/pnas.0403010101
[22]	Lewis A L, Cao H Z, Patel S K, et al. NeuA sialic acid O-acetylesterase activity modulates O-acetylation of capsular polysaccharide in group B Streptococcus[J]. Journal of Biological Chemistry, 2007, 282(38): 27562-27571. doi: 10.1074/jbc.M700340200
[23]	Dong J J, Wei Y Z, Ye X, et al. Discovery and expression of 3 siglecs-like in Oreochromis niloticus neutrophil, and their interaction with group B streptococcal sialylated capsular polysaccharides[J]. Molecular Immunology, 2016, 73: 158-169. doi: 10.1016/j.molimm.2016.01.005
[24]	Kayansamruaj P, Pirarat N, Hirono I, et al. Increasing of temperature induces pathogenicity of Streptococcus agalactiae and the up-regulation of inflammatory related genes in infected Nile tilapia (Oreochromis niloticus)[J]. Veterinary Microbiology, 2014, 172(1-2): 265-271. doi: 10.1016/j.vetmic.2014.04.013
[25]	van Calsteren M R, Gagnon F, Lacouture S, et al. Structure determination of Streptococcus suis serotype 2 capsular polysaccharide[J]. Biochemistry and Cell Biology, 2010, 88(3): 513-525. doi: 10.1139/O09-170
[26]	Guidolin A, Morona J K, Morona R, et al. Nucleotide sequence analysis of genes essential for capsular polysaccharide biosynthesis in Streptococcus pneumoniae type 19F[J]. Infection and Immunity, 1994, 62(12): 5384-5396.
[27]	Minic Z, Marie C, Delorme C, et al. Control of EpsE, the phosphoglycosyltransferase initiating exopolysaccharide synthesis in Streptococcus thermophilus, by EpsD tyrosine kinase[J]. Journal of Bacteriology, 2007, 189(4): 1351-1357. doi: 10.1128/JB.01122-06
[28]	Kemp B P, Horne J, Bryant A, et al. Xanthomonas axonopodis pv. manihotis gumD gene is essential for EPS production and pathogenicity and enhances epiphytic survival on cassava (Manihot esculenta)[J]. Physiological and Molecular Plant Pathology, 2004, 64(4): 209-218. doi: 10.1016/j.pmpp.2004.08.007
[29]	Shainheit M G, Mulé M, Camilli A. The core promoter of the capsule operon of Streptococcus pneumoniae is necessary for colonization and invasive disease[J]. Infection and Immunity, 2014, 82(2): 694-705. doi: 10.1128/IAI.01289-13
[30]	Rosini R, Campisi E, De Chiara M, et al. Genomic analysis reveals the molecular basis for capsule loss in the group B Streptococcus population[J]. PLoS One, 2015, 10(5): e0125985. doi: 10.1371/journal.pone.0125985
[31]	Chaffin D O, McKinnon K, Rubens C E. CpsK of Streptococcus agalactiae exhibits α2,3-sialyltransferase activity in Haemophilus ducreyi[J]. Molecular Microbiology, 2002, 45(1): 109-122. doi: 10.1046/j.1365-2958.2002.02988.x
[32]	Chen M, Wang R, Luo F G, et al. Streptococcus agalactiae isolates of serotypes Ia, III and V from human and cow are able to infect tilapia[J]. Veterinary Microbiology, 2015, 180(1-2): 129-135. doi: 10.1016/j.vetmic.2015.07.033
[33]	Pereira U P, Mian G F, Oliveira I C M, et al. Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia[J]. Veterinary Microbiology, 2010, 140(1-2): 186-192. doi: 10.1016/j.vetmic.2009.07.025
[34]	刘志刚, 可小丽, 卢迈新, 等. 温度对尼罗罗非鱼无乳链球菌毒力的影响[J]. 水产学报, 2013, 37(11): 1733-1741. Liu Z G, Ke X L, Lu M X, et al. Effect of temperature on the virulence of Streptococcus agalactiae from Nile tilapia (Oreochromis niloticus)[J]. Journal of Fisheries of China, 2013, 37(11): 1733-1741 (in Chinese).
[35]	Mereghetti L, Sitkiewicz I, Green N M, et al. Remodeling of the Streptococcus agalactiae transcriptome in response to growth temperature[J]. PLoS One, 2008, 3(7): e2785. doi: 10.1371/journal.pone.0002785
[36]	Beaussart A, Péchoux C, Trieu-Cuot P, et al. Molecular mapping of the cell wall polysaccharides of the human pathogen Streptococcus agalactiae[J]. Nanoscale, 2014, 6(24): 14820-14827. doi: 10.1039/C4NR05280C
[37]	石洁, 李先富, 张先云, 等. 荚膜唾液酸缺失对2型猪链球菌与人单核细胞相互作用的影响[J]. 免疫学杂志, 2011, 27(11): 926-930. Shi J, Li X F, Zhang X Y, et al. The absence of sialylation effects the interactions between Streptococcus suis serotype 2 and human THP-1 monocytes[J]. Immunological Journal, 2011, 27(11): 926-930 (in Chinese).
[38]	Carlin A F, Uchiyama S, Chang Y C, et al. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response[J]. Blood, 2009, 113(14): 3333-3336. doi: 10.1182/blood-2008-11-187302
[39]	Bouchet V, Hood D W, Li J J, et al. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media[J]. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(15): 8898-8903. doi: 10.1073/pnas.1432026100

[1]	MA Shuang, JIANG Mi, LI Yanhong, LIU Yang, SUN Yu, TANG Xiaoqi, WU Zhengli. Pathogenicity and inactivated vaccine protection of Staphylococcus sciuri JS-1 on Carassius auratus[J]. Journal of fisheries of china, 2022, 46(9): 1669-1679. DOI: 10.11964/jfc.20210712969
[2]	SUN Yiru, ZHANG Hongyan, BI Yihui, MA Sisi, ZHANG Kai, JI Jie, WANG Tao, JIA Yongyi, YIN Shaowu. Molecular characteristics and expression pattern analysis under pathogen stress of SOCSs genes in three species of yellow catfish[J]. Journal of fisheries of china, 2022, 46(9): 1537-1552. DOI: 10.11964/jfc.20201012465
[3]	WANG Qiaohuang, LIN Nan, YUAN Lihua, JI Jing, LIN Dan. Isolation, identification, major virulence genes and pathogenicity of Yersinia ruckeri from Micropterus salmoides[J]. Journal of fisheries of china, 2022, 46(5): 825-835. DOI: 10.11964/jfc.20220213326
[4]	CHEN Qiang, LI Yingying, YANG Jinxian, SONG Tieying, GE Junqing. Pathogenicity of Anguillid herpesvirus to Anguilla anguilla[J]. Journal of fisheries of china, 2021, 45(6): 940-947. DOI: 10.11964/jfc.20200812370
[5]	CHAI Jingru, WANG Di, LU Tongyan, CAO Yongsheng, LI Shaowu. Isolation, identification and pathogenicity of Flavobacterium psychrophilum from Oncorhynchus mykiss[J]. Journal of fisheries of china, 2021, 45(6): 929-939. DOI: 10.11964/jfc.20200512260
[6]	LI Jinjin, HONG Baohua, NI Sizhen, BAO Jiawei, MA Rongrong, YIN Fei, HE Jie, LUO Huaming, LI Chen, HUANG Yuanming, QIAN Dong. Isolation, identification and pathogenicity analysis of luminous Vibrio campbellii from Litopenaeus vannamei[J]. Journal of fisheries of china, 2021, 45(4): 600-612. DOI: 10.11964/jfc.20200112121
[7]	LIU Xiaofang, REN Yan, ZHANG Defeng, GONG Hua, SHI Cunbin, CHANG Ouqin, PAN Houjun. Detection, genotyping and pathogenicity of virulence genes in Aeromonas species isolated from diseased freshwater fish[J]. Journal of fisheries of china, 2021, 45(3): 462-471. DOI: 10.11964/jfc.20200312180
[8]	LI Wenyue, ZUO Zhihan, ZHANG Jingjing, SHANG Bijiao, SUN Jinsheng. Isolation and identification of pathogens of ulcer disease in Cynoglossus semilaevis[J]. Journal of fisheries of china, 2020, 44(4): 672-680. DOI: 10.11964/jfc.20190711874
[9]	ZHANG Honghu, YUAN Na, FU Chaoying, HE Jie, LUO Huaming, BAO Jiawei, QIAN Dong. Isolation, identification and pathogenicity studies on visceral granulomatous disease in Acanthopagrus schlegelii[J]. Journal of fisheries of china, 2019, 43(12): 2554-2566. DOI: 10.11964/jfc.20181011489
[10]	JIAO Kaiqiang, WANG Yingeng, RONG Xiaojun, CHEN Jia, ZHANG Zheng, LIAO Meijie, LI Bin, SUN Luyu, SU Yuezhong. Pathogenicity of Cryptocaryon irritans to Larimichthys crocea and Chinese herbal inhibition on the parasitic generation reproduction[J]. Journal of fisheries of china, 2019, 43(5): 1326-1337. DOI: 10.11964/jfc.20180311206

Cited By

Cited by

Periodical cited type(1)

孟可心，高海燕，曹蒙，宋孟迪，姜继凯，曾洁. 无乳链球菌产CMP-唾液酸合成酶发酵培养基优化. 食品工业科技. 2019(22): 138-143+150 .

Other cited types(4)

Get Citation

PDF in Chinese

XML

Article views (1271) PDF downloads (5) Cited by(5)

Expressions of capsular polysaccharide synthetic gene of Streptococcus agalactiae isolated from Nile tilapia(Oreochromis niloticus) and their effects on capsular sialic acid content and bacterial pathogenicity

Abstract

References

Related Articles

Cited by

Periodical cited type(1)

Other cited types(4)

Catalog

Related

Expressions of capsular polysaccharide synthetic gene of Streptococcus agalactiae isolated from Nile tilapia(Oreochromis niloticus) and their effects on capsular sialic acid content and bacterial pathogenicity

Abstract

References

Related Articles

Cited by

Periodical cited type(1)

Other cited types(4)

Catalog

Related

Export File

Citation

Format

Content