Population genomics study of Vibrio alginolyticus
Received date: 2021-02-09
Revised date: 2021-03-16
Online published: 2021-03-30
Supported by
Supported by the National Key R&D Program Nos of China(2018YFC1603902);Supported by the National Key R&D Program Nos of China(2017YFC1601500);China Postdoctoral Science Foundation No(2020M672836)
Vibrio alginolyticus is a Gram-negative bacillus that causes vibriosis to human and aquatic products, including fish, shrimp and shellfish. It poses a threat to public health and causes enormous economic losses to the aquaculture industry. However, research on genetic diversity and pathogenicity-related genetic elements based on whole genome is still lacking. In this study, sixty-eight strains of V. alginolyticus were collected from four provinces of China and the whole genome sequences were obtained. Combined with 113 publicly available genome sequences downloaded from NCBI, we inferred the population structure of V. alginolyticus by using fineSTRUCTURE software, and identified the virulence and antibiotic resistance factors using the VFDB, CARD and ResFinder database. The results indicated that V. alginolyticus included two main lineages, named Lineage 1 and Lineage 2. Both lineages distributed in America and Asia, but all the European genomes were classified into Lineage 1. A single cross-ocean transmission event was inferred from one of the 12 identified clonal groups in our dataset. V. alginolyticus genome contains a variety of virulence factors, such as tlh, OmpU, and IlpA, etc. The distribution of virulence factors revealed no lineage-specificity, but some of which revealed differences in their geographical distribution. A lower frequency of VP1611, vcrD, vopD, fleR/flrC and a higher frequency of IlpA were observed in genomes of Europe than other continents. In China, a lower frequency of fleR/flrC, and no IlpA were observed in genomes from Guangxi province. Among the identified antibiotic resistance genes, TxR and fos are significantly enriched in Lineage 2. In addition, TxR is more common in genomes from Asia, compared with the American and European genomes. But in China, the frequency of TxR in Sichuan genomes is much lower than in other provinces. We also found that large fragments of plasmids or ICEs that carried multiple drug resistance genes were present in five V. alginolyticus genomes (VA24, VA28, 2014V-1011, ZJ-T and Vb1833). Based on population genomics analysis, our study delineated the population structure, distribution of virulence and antibiotic resistance related factors of V. alginolyticus, which lays a foundation for future study of genetic characters and pathogenesis mechanism of this pathogen and will improve the works on monitoring, prevention and control of this pathogen.
Hongyuan Zheng, Lin Yan, Chao Yang, Yarong Wu, Jingliang Qin, Tongyu Hao, Dajin Yang, Yunchang Guo, Xiaoyan Pei, Tongyan Zhao, Yujun Cui . Population genomics study of Vibrio alginolyticus[J]. Hereditas(Beijing), 2021 , 43(4) : 350 -361 . DOI: 10.16288/j.yczz.21-061
| [1] | Lajnef R, Snoussi M, Romalde JL, Nozha C, Hassen A. Comparative study on the antibiotic susceptibility and plasmid profiles of Vibrio alginolyticus strains isolated from four Tunisian marine biotopes. World J Microbiol Biotechnol, 2012,28(12):3345-3363. |
| [2] | Xie JS, Bu LF, Jin S, Wang XY, Zhao QS, Zhou SM, Xu YJ. Outbreak of vibriosis caused by Vibrio harveyi and Vibrio alginolyticus in farmed seahorse Hippocampus kuda in China. Aquaculture, 2020,523:735168. |
| [3] | Reilly GD, Reilly CA, Smith EG, Baker-Austin C. Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Euro Surveill, 2011,16(42):19994. |
| [4] | Zhou K, Sun F, Zha DJ, Liu JY, Ma YY, Hao XK, Xu XL . Biological characteristics of a Vibrio alginolyticus strain isolated from a patient with chronic otitis externa. J Pathog Biol, 2020,158(2):146-151. |
| [4] | 周柯, 孙菲, 查定军, 刘家云, 马越云, 郝晓柯, 徐修礼 . 慢性外耳道炎患者分离溶藻弧菌的鉴定及生物学特性分析. 中国病原生物学杂志, 2020,158(2):146-151. |
| [5] | Gómez-León J, Villamil L, Lemos ML, Novoa B, Figueras A. Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Appl Environ Microbiol, 2005,71(1):98-104. |
| [6] | González-Escalona N, Blackstone GM, Depaola A. Characterization of a Vibrio alginolyticus strain, isolated from Alaskan oysters, carrying a hemolysin gene similar to the thermostable direct hemolysin-related hemolysin gene (trh) of Vibrio parahaemolyticus. Appl Environ Microbiol, 2006,72(12):7925-7929. |
| [7] | Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE. Increasing rates of vibriosis in the United States, 1996-2010: review of surveillance data from 2 systems. Clin Infect Dis, 2012, 54 Suppl 5(05): S391-S395. |
| [8] | Jacobs Slifka KM, Newton AE, Mahon BE. Vibrio alginolyticus infections in the USA, 1988-2012. Epidemiol Infect, 2017,145(7):1491-1499. |
| [9] | Hu NX, Ma C, Li YJ . Research progress on molecular typing technology of Vibrio alginolyticus. Int J Lab Med, 2014,35(13):1753-1755. |
| [9] | 胡南霞, 马聪, 李艳君 . 溶藻弧菌分子分型技术的研究进展. 国际检验医学杂志, 2014,35(13):1753-1755. |
| [10] | Sudheesh PS, Jie K, Xu HS. Random amplified polymorphic DNA-PCR typing of Vibrio parahaemolyticus and V. alginolyticus isolated from cultured shrimps. Aquaculture, 2002,207(1-2):11-17. |
| [11] | Ouyang JL, Zhou YC, Wu YG, Dai XL, Wang SF, Xie ZY . RAPD analysis of genetic diversity of Vibrio alginolyticus isolated from Hainan province. Marin Sci, 2011,35(7):30-36. |
| [11] | 欧阳吉隆, 周永灿, 吴学贵, 戴小连, 王世锋, 谢珍玉 . 海南地区溶藻弧菌遗传多样性的RAPD分析. 海洋科学, 2011,35(7):30-36. |
| [12] | Ren CH, Hu CQ, Luo P, Chen C, Jiang X, Wang QB. Genotyping of Vibrio alginolyticus isolates from Daya Bay by infrequent-restriction-site PCR and pulsed-field gel electrophoresis. Mol Cell Probes, 2008,22(4):267-271. |
| [13] | Talon D, Cailleaux V, Thouverez M, Michel-Briand Y. Discriminatory power and usefulness of pulsed-field gel electrophoresis in epidemiological studies of Pseudomonas aeruginosa. J Hosp Infect, 1996,32(2):135-145. |
| [14] | Inglis TJ, Garrow SC, Adams C, Henderson M, Mayo M, Currie BJ. Acute melioidosis outbreak in Western Australia. Epidemiol Infect, 1999,123(3):437-443. |
| [15] | Xie ZY, Hu CQ, Chen C, Zhang LP, Ren CH. Investigation of seven Vibrio virulence genes among Vibrio alginolyticus and Vibrio parahaemolyticus strains from the coastal mariculture systems in Guangdong, China. Lett Appl Microbiol, 2005,41(2):202-207. |
| [16] | Hernández-Robles MF, álvarez-Contreras AK, Juárez- García P, Natividad-Bonifacio I, Curiel-Quesada E, Vázquez-Salinas C, Qui?ones-Ramírez EI. Virulence factors and antimicrobial resistance in environmental strains of Vibrio alginolyticus. Int Microbiol, 2016,19(4):191-198. |
| [17] | Mechri B, Medhioub A, Medhioub MN, Aouni M. Genotypic diversity, antimicrobial resistance and screening of Vibrio cholerae molecular virulence markers in Vibrio alginolyticus strains recovered from a Tunisian Ruditapes decussatus hatchery. Pol J Microbiol, 2013,62(3):263-272. |
| [18] | Wei S . Detection of Vibrio alginolyticus and its virulence- related genes[Dissertation]. Jinan University, 2013. |
| [18] | 魏霜 . 溶藻弧菌及其毒力相关基因的检测[学位论文]. 暨南大学, 2013. |
| [19] | Xian YY . Analysis of the distribution of virulence-related genes and antibiotic resistance of Vibrio parahaemolyticus and Vibrio alginolyticus[Dissertation]. Jinan University, 2015. |
| [19] | 冼钰茵 . 副溶血弧菌与溶藻弧菌毒力基因分布与抗生素耐药性分析[学位论文]. 暨南大学, 2015. |
| [20] | Mechri B, Monastiri A, Medhioub A, Medhioub MN, Aouni M. Molecular characterization and phylogenetic analysis of highly pathogenic Vibrio alginolyticus strains isolated during mortality outbreaks in cultured Ruditapes decussatus juvenile. Microb Pathog, 2017,111:487-496. |
| [21] | Chen HQ . Analysis of drug resistance and drug resistance genes of a pathogenic Vibrio alginolyticus from large yellow croaker. Fish Info & Strateg, 2020,35(1):63-67. |
| [21] | 陈洪清 . 一株大黄鱼致病性溶藻弧菌的耐药性及耐药基因分析. 渔业信息与战略, 2020,35(1):63-67. |
| [22] | Limmathurotsakul D, Golding N, Dance DAB, Messina JP, Pigott DM, Moyes CL, Rolim DB, Bertherat E, Day NPJ, Peacock SJ, Hay SI. Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol, 2016,1:15008. |
| [23] | Chewapreecha C, Holden MTG, Vehkala M, V?lim?ki N, Yang ZR, Harris SR, Mather AE, Tuanyok A, De Smet B, Le Hello S, Bizet C, Mayo M, Wuthiekanun V, Limmathurotsakul D, Phetsouvanh R, Spratt BG, Corander J, Keim P, Dougan G, Dance DAB, Currie BJ, Parkhill J, Peacock SJ. Global and regional dissemination and evolution of Burkholderia pseudomallei. Nat Microbiol, 2017,2:16263. |
| [24] | Yang C, Pei XY, Wu YR, Yan L, Yan YF, Song YQ, Coyle NM, Martinez-Urtaza J, Quince C, Hu QH, Jiang M, Feil E, Yang DJ, Song YJ, Zhou DS, Yang RF, Falush D, Cui YJ. Recent mixing of Vibrio parahaemolyticus populations. Isme J, 2019,13(10):2578-2588. |
| [25] | Yang C, Zhang XL, Fan H, Li YH, Hu QH, Yang RF, Cui YJ. Genetic diversity, virulence factors and farm-to-table spread pattern of Vibrio parahaemolyticus food-associated isolates. Food Microbiol, 2019,84:103270. |
| [26] | Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet, 2012,8(1):e1002453. |
| [27] | Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 2014,30(15):2114-2120. |
| [28] | Cui YJ, Yu C, Yan YF, Li DF, Li YJ, Jombart T, Weinert LA, Wang ZY, Guo ZB, Xu LZ, Zhang YJ, Zheng HC, Qin N, Xiao X, Wu MS, Wang XY, Zhou DS, Qi ZZ, Du ZM, Wu HL, Yang XW, Cao HZ, Wang H, Wang J, Yao SS, Rakin A, Li YR, Falush D, Balloux F, Achtman M, Song YJ, Wang J, Yang RF. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc Natl Acad Sci USA, 2013,110(2):577-582. |
| [29] | Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics, 2003,0(1): 10.3.1-10.3.18. |
| [30] | Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics, 2014,30(14):2068-2069. |
| [31] | Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics, 2015,31(22):3691-3693. |
| [32] | Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res, 2016,44(W1):W242-W245. |
| [33] | Liu B, Zheng DD, Jin Q, Chen LH, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res, 2019,47(D1):D687-D692. |
| [34] | Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, Huynh W, Nguyen ALV, Cheng AA, Liu SH, Min SY, Miroshnichenko A, Tran HK, Werfalli RE, Nasir JA, Oloni M, Speicher DJ, Florescu A, Singh B, Faltyn M, Hernandez-Koutoucheva A, Sharma AN, Bordeleau E, Pawlowski AC, Zubyk HL, Dooley D, Griffiths E, Maguire F, Winsor GL, Beiko RG, Brinkman FSL, Hsiao WWL, Domselaar GV, Mcarthur AG. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res, 2020,48(D1):D517-D525. |
| [35] | Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, Philippon A, Allesoe RL, Rebelo AR, Florensa AF, Fagelhauer L, Chakraborty T, Neumann B, Werner G, Bender JK, Stingl K, Nguyen M, Coppens J, Xavier BB, Malhotra-Kumar S, Westh H, Pinholt M, Anjum MF, Duggett NA, Kempf I, Nyk?senoja S, Olkkola S, Wieczorek K, Amaro A, Clemente L, Mossong J, Losch S, Ragimbeau C, Lund O, Aarestrup FM. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother, 2020,75(12):3491-3500. |
| [36] | Wang HQ, Yang C, Sun Z, Zheng W, Zhang W, Yu H, Wu YR, Didelot X, Yang RF, Pan JC, Cui YJ. Genomic epidemiology of Vibrio cholerae reveals the regional and global spread of two epidemic non-toxigenic lineages. PLoS Negl Trop Dis, 2020,14(2):e0008046. |
| [37] | Cui YJ, Yang C, Qiu HL, Wang H, Yang RF, Falush D. The landscape of coadaptation in Vibrio parahaemolyticus. eLife, 2020,9:e54136. |
| [38] | Zhao Z, Liu JX, Deng YQ, Huang W, Ren CH, Call DR, Hu CQ. The Vibrio alginolyticus T3SS effectors, Val1686 and Val1680, induce cell rounding, apoptosis and lysis of fish epithelial cells. Virulence, 2018,9(1):318-330. |
| [39] | Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet, 2003,361(9359):743-749. |
| [40] | Zhou XH, Konkel ME, Call DR. Type III secretion system 1 of Vibrio parahaemolyticus induces oncosis in both epithelial and monocytic cell lines. Microbiology (Reading), 2009,155(Pt 3):837-851. |
| [41] | Burdette DL, Seemann J, Orth K. Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis. Mol Microbiol, 2009,73(4):639-649. |
| [42] | Jia AR, Woo NYS, Zhang XH. Expression, purification, and characterization of thermolabile hemolysin (TLH) from Vibrio alginolyticus. Dis Aquat Organ, 2010,90(2):121-127. |
| [43] | Wong SK, Zhang XH, Woo NYS. Vibrio alginolyticus thermolabile hemolysin(TLH)induces apoptosis, membrane vesiculation and necrosis in sea bream erythrocytes. Aquaculture, 2012,330-333:29-36. |
| [44] | Cai SH, Yaol SY, Lu YS, Wu ZH, Jian JC, Wang B. Immune response in Lutjanus erythropterus induced by the major outer membrane protein (OmpU) of Vibrio alginolyticus. Dis Aquat Organ, 2010,90(1):63-68. |
| [45] | Lv TT, Dai F, Zhuang QT, Zhao XL, Shao YN, Guo M, Lv ZM, Li CH, Zhang WW. Outer membrane protein OmpU is related to iron balance in Vibrio alginolyticus. Microbiol Res, 2020,230:126350. |
| [46] | Cambray G, Guerout AM, Mazel D. Integrons. Annu Rev Genet, 2010,44:141-166. |
| [47] | Rajpara N, Nair M, Bhardwaj AK. A highly promiscuous integron, plasmids, extended spectrum beta lactamases and efflux pumps as factors governing multidrug resistance in a highly drug resistant Vibrio fluvialis isolate BD146 from Kolkata, India. Indian J Microbiol, 2018,58(1):60-67. |
/
| 〈 |
|
〉 |
www.chinagene.cn
备案号：京ICP备09063187号
