Pathogenicity and whole genome analysis of a Nocardia seriolae strain isolated from snakehead
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    Abstract:

    [Background] The infection of Nocardia seriolae, a typical opportunistic pathogen, has been documented in many kinds of fishes such as Channa argus and Micropterus salmoides, particularly wounded fishes or fishes with decreased immunity. The resulted nocardiosis lasts a long time, causing great loss to the aquaculture. [Objective] This paper aims to clarify the pathogenicity of Nocardia seriolae isolated from hybrid snakehead (C. maculata♀×C. argus), as well as the whole genome and virulence factors information of the pathogen, which is expected to lay a basis for the future research on etiology ofNocardia seriolae, prevention and control of this pathogen, and vaccine development. [Methods] Through challenge test and pathological analysis of target snakehead organs, the virulence and pathogenic characteristics of Nocardia seriolae NK201610020 were elucidated. In addition, based on whole-genome sequencing and comparative genomics analysis, the genomic features and virulence genes information of the strain were clarified. [Results] The result of challenge test showed that the death rates in the five infection groups were up to over 90% except the group of 1.5×103, and the LD50is1.079×103 CFU/mL, which indicating the strong virulence of the strain. Histopathological results revealed serious pathological damages in liver, spleen, and kidney, as well as formation of granulomas. The whole genome of NK201610020 was 8 294 329 bp with GC content of 68.10% and 7 812 coding genes. The genomes of Nocardia seriolae from different hosts and different regions showed little difference (>99.9% similarity). According to the alignment with virulence gene database, 171 coding genes in the genome of NK201610020 might be virulence genes, which were involved in cell wall synthesis, nutrient metabolism, and persistent bacterial infection. [Conclusion] Nocardia seriolae has strong virulence, and conserved genome sequence containing diverse virulence genes. The results lay a basis for further analysis of Nocardia seriolae pathogenic mechanism.

    Reference
    [1] 张建丽,刘志恒.诺卡氏菌型放线菌的分类[J].微生物学报, 2001, 41(4):513-517 Zhang JL, Liu ZH. Taxonomy of the nocardioform actinomycetes[J]. Acta Microbiologica Sinica, 2001, 41(4):513-517(in Chinese)
    [2] Shimahara Y, Huang YF, Tsai MA, Wang PC, Yoshida T, Lee JL, Chen SC. Genotypic and phenotypic analysis of fish pathogen, Nocardia seriolae, isolated in Taiwan[J]. Aquaculture, 2009, 294(3/4):165-171
    [3] Wang GL, Yuan SP, Jin S. Nocardiosis in large yellow croaker, Larimichthys crocea (Richardson)[J]. Journal of Fish Diseases, 2005, 28(6):339-345
    [4] 王国良,徐益军,金珊,祝璟琳,朱文渊.养殖乌鳢诺卡氏菌病及其病原研究[J].水生生物学报, 2009, 33(2):277-283 Wang GL, Xu YJ, Jin S, Zhu JL, Zhu WY. Research on the nocardiosis and pathogen in reared snakehead, ophiocephalus Argus cantor[J]. Acta Hydrobiologica Sinica, 2009, 33(2):277-283(in Chinese)
    [5] Itano T, Kawakami H, Kono T, Sakai M. Estimation of the time for Nocardia seriolae infection of cultured yellowtail[J]. Fish Pathology, 2008, 43(2):86-88
    [6] Han HJ, Kwak MJ, Ha SM, Yang SJ, Kim JD, Cho KH, Kim TW, Cho MY, Kim BY, Jung SH, et al. Genomic characterization of Nocardia seriolae strains isolated from diseased fish[J]. MicrobiologyOpen, 2019, 8(3):e00656
    [7] 黄郁葱,简纪常,吴灶和,鲁义善,余坦健.卵形鲳鲹结节病病原的分离与鉴定[J].广东海洋大学学报, 2008, 28(4):49-53 Huang YC, Jian JC, Wu ZH, Lu YS, Yu TJ. Isolation and identification of the pathogen causing sarcoidosis of Trachinotus ovatus[J]. Journal of Guangdong Ocean University, 2008, 28(4):49-53(in Chinese)
    [8] 2021年中国渔业统计年鉴[M].北京:中国农业出版社. 2021:30-33 China Fishery Statisical Yearbook[M]. Bei Jing:China Agriculture Press. 2021:30-33
    [9] Isik K, Chun J, Hah YC, Goodfellow M. Nocardia salmonicida nom. rev., a fish pathogen[J]. International Journal of Systematic Bacteriology, 1999, 49(Pt 2):833-837
    [10] Bransden MP, Carson J, Munday BL, Handlinger JH, Carter CG, Nowak BF. Nocardiosis in tank-reared Atlantic salmon, Salmo salar L.[J]. Journal of Fish Diseases, 2000, 23(1):83-85
    [11] 满其蒙.鰤鱼诺卡氏菌致病机制的研究[D].上海:上海海洋大学硕士学位论文, 2013 Man QM. Studies on pathogenic mechanism of Nocardia seriolae[D]. Shanghai:Master's Thesis of Shanghai Ocean University, 2013(in Chinese)
    [12] Strauss EJ, Falkow S. Microbial pathogenesis:genomics and beyond[J]. Science, 1997, 276(5313):707-712
    [13] Yasuike M, Nishiki I, Iwasaki Y, Nakamura Y, Fujiwara A, Shimahara Y, Kamaishi T, Yoshida T, Nagai S, Kobayashi T, et al. Analysis of the complete genome sequence of Nocardia seriolae UTF1, the causative agent of fish nocardiosis:the first reference genome sequence of the fish pathogenic Nocardia species[J]. PLoS One, 2017, 12(3):e0173198
    [14] Xia LQ, Cai J, Wang B, Huang YC, Jian JC, Lu YS. Draft genome sequence of Nocardia seriolae ZJ0503, a fish pathogen isolated from Trachinotus ovatus in China[J]. Genome Announcements, 2015, 3(1):e01223-e01214
    [15] 曹阅,陈立志,刘晓颖,冯二凯,汪孙杰,徐晶,冯卓.坏死梭杆菌斑马鱼模型建立与LD50的测定[J].特产研究, 2012, 34(1):14-18 Cao Y, Chen LZ, Liu XY, Feng EK, Wang SJ, Xu J, Feng Z. Establishment of zebrafish model with Fusobacterium necrophorum biotype AB and determination of LD50[J]. Special Wild Economic Animal and Plant Research, 2012, 34(1):14-18(in Chinese)
    [16] Sundararajan S, Muniyan R. Latent tuberculosis:interaction of virulence factors in Mycobacterium tuberculosis[J]. Molecular Biology Reports, 2021, 48(8):6181-6196
    [17] Quadri LE, Sello J, Keating TA, Weinreb PH, Walsh CT. Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin[J]. Chemistry&Biology, 1998, 5(11):631-645
    [18] 王旸,肖春玲.以异柠檬酸裂解酶为靶点筛选抗持留结核分枝杆菌药物[J].中国抗生素杂志, 2007, 32(7):391-395 Wang Y, Xiao CL. Isocitrate lyase, a new target in anti-tuberculosis drug research[J]. Chinese Journal of Antibiotics, 2007, 32(7):391-395(in Chinese)
    [19] Ganapathy U, Marrero J, Calhoun S, Eoh H, de Carvalho LPS, Rhee K, Ehrt S. Two enzymes with redundant fructose bisphosphatase activity sustain gluconeogenesis and virulence in Mycobacterium tuberculosis[J]. Nature Communications, 2015, 6:7912
    [20] TA Weinreb PH, Walsh CT. Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin[J]. Chemistry&Biology, 1998, 5(11):631-645,
    [21] Menozzi FD, Rouse JH, Alavi M, Laude-Sharp M, Muller J, Bischoff R, Brennan MJ, Locht C. Identification of a heparin-binding hemagglutinin present in mycobacteria[J]. The Journal of Experimental Medicine, 1996, 184(3):993-1001
    [22] Saini V, Farhana A, Steyn AJC. Mycobacterium tuberculosis WhiB3:a novel iron-sulfur cluster protein that regulates redox homeostasis and virulence[J]. Antioxidants&Redox Signaling, 2012, 16(7):687-697
    [23] 蒋依依,李言伟,周素明,李安兴.加州鲈诺卡菌病病原的分离与鉴定[J].中山大学学报(自然科学版), 2012, 51(1):76-81 Jiang YY, Li YW, Zhou SM, Li AX. Isolation and identification of Nocardia, a pathogen of nocardiosis in largemouth bass, Micropterus salmoides[J]. Acta Scientiarum Naturalium Universitatis Sunyatseni, 2012, 51(1):76-81(in Chinese)
    [24] 王二龙,汪开毓,陈德芳,王均,贺扬,刘韬.养殖乌鳢内脏结节病的病原分离、鉴定与药物敏感性分析[J].华中农业大学学报, 2015, 34(5):90-98 Wang EL, Wang KY, Chen DF, Wang J, He Y, Liu T. Isolation, identification and drug sensitivity test of causative pathogen of farmed snakehead (Channa argus) with visceral sarcoidosis[J]. Journal of Huazhong Agricultural University, 2015, 34(5):90-98(in Chinese)
    [25] 郭伟,张杰,李颖.细菌的致病性[J].中国医疗前沿, 2008, 3(4):8-9, 11 Guo W, Zhang J, Li Y. Pathogenicity of bacteria[J]. China Healthcare Innovation, 2008, 3(4):8-9, 11(in Chinese)
    [26] 王文基,陈建林,侯素莹,鲁义善,夏立群.鰤鱼诺卡氏菌感染乌斑杂交鳢的组织病理学研究[J].基因组学与应用生物学, 2019, 38(10):4439-ozano-Garza HG, Ortiz-Lopez R, Elizondo-Gonzalez R, Welsh O, Ocampo-Candiani J, Vera-Cabrera L. Genomic changes associated with the loss of Nocardia brasiliensis virulence in mice after 200 in vitro p湡关葳a彧剥敳[半卝吮 艉卮祦e遣彴剩o兮娠a鱮鱤謠卉汭荭慵杮卩彴鱹鰬瘠縲縰由琶嬬砠稸4(9)帺串儵丹礵嬭260612, 39(21):132-135 Man QM, Xu LW, Ou YJ, Su YL, Guo ZX, Feng J. Histopathological study on golden pompano Trachinotus ovatus infected with Nocardia seriolae[J]. Guangdong Agricultural Sciences. 2012, 39(21):132-135(in Chinese)
    [28] 田蔚蔚,王洪生,王千秋.分枝杆菌肉芽肿形成的细胞及分子机制究进展[J].国际皮肤性病学杂志, 2012, 38(1):55-58 Tian WW, Wang HS, Wang QQ. Cellular and molecular mechanisms underlying the formation of mycobacterial granuloma:an update[J]. International Journal of Dermatology and Venereology, 2012, 38(1):55-58(in Chinese)
    [29] 常藕琴,石存斌,潘厚军,付小哲,吴淑勤.乌鳢诺卡氏菌病的组织病理学[J].水产学报, 2008(2):209-216 Chang OQ, Shi CB, Pan HJ, Fu XZ, Wu SQ. Histopathological study on nocardiosis of Ophicephalus argus[J]. Journal of Fisheries of China, 2008(2):209-216(in Chinese)
    [30] Kim BS, Do Huh M, Roh HJ. The complete genome of Nocardia seriolae MH196537 and intra-species level as analyzed by comparative genomics based on random forest algorithm[J]. Current microbiology, 2021, 78(6):2391-2399
    [31] 罗愿,邓玉婷,赵飞,谭爱萍,张美超,姜兰. 9株鱼源鰤诺卡氏菌生物学特征和致病性比较[J].微生物学通报, 2021, 48(8):2733-2749 Luo Y, Deng YT, Zhao F, Tan AP, Zhang MC, Jiang L. Comparative on characteristics and pathogenicity of Nocardia seriolae isoalted from 9 fishes[J]. Microbiology China, 2021, 48(8):2733-2749(in Chinese)
    [32] 孙丕,梅建.结核分枝杆菌中的分枝菌酸[J].中国防痨杂志, 2010, 32(7):397-402 Sun P, Mei J. Study on mycolic acid in Mycobacterium tuberculosis[J]. Chinese Journal of Antituberculosis, 2010, 32(7):397-402(in Chinese)
    [33] Wiker HG, Harboe M. The antigen 85 complex:a major secretion product of Mycobacterium tuberculosis[J]. Emerging Infectious Diseases, 1992, 56(4):648-661
    [34] Belisle JT, Vissa VD, Sievert T, Takayama K, Brennan PJ, Besra GS. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis[J]. Science, 1997, 276(5317):1420-1422
    [35] Itano T, Nakaoka N, Kawakami H, Kono T, Sakai M. Comparison of sensitivity between Yellowtail Seriola quinqueradiata and Red Sea Bream Pagrus major to Nocardia seriolae[J]. Fish Pathology, 2006, 41(4):135-139
    [36] Hemati Z, Derakhshandeh A, Haghkhah M, Chaubey KK, Gupta S, Singh M, Singh SV, Dhama K. Mammalian cell entry operons; novel and major subset candidates for diagnostics with special reference to Mycobacterium avium sub species paratuberculosis infection[J]. Veterinary Quarterly, 2019, 39(1):65-75
    [37] Casali N, White AM, Riley LW. Regulation of the Mycobacterium tuberculosis mce1 operon[J]. Journal of Bacteriology, 2006, 188(2):441-449
    [38] 徐广贤.牛结核分枝杆菌Mce4A和Mce4E蛋白与牛肺泡巨噬细胞相互作用的研究[D].北京:中国农业大学博士学位论文, 2007 Xu GX. Research on interaction of Mycobacterium Bovis proteins Mce4A and Mce4E with bovine alveolar macrophage[D]. Beijing:Doctoral Dissertation of China Agricultural University, 2007(in Chinese)
    [39] Shukla H, Kumar V, Singh AK, Rastogi S, Khan SR, Siddiqi MI, Krishnan MY, Akhtar MS. Isocitrate lyase of Mycobacterium tuberculosis is inhibited by quercetin through binding at N-terminus[J]. International Journal of Biological Macromolecules, 2015, 78:137-141
    [40] 徐水凌,徐妍,黄佳,范宏彦,金梦媚.磷脂酶C分子在结核分枝杆菌触发树突状细胞细胞骨架重排中的作用[J].浙江大学学报(医学版), 2013, 42(2):184-191 Xu SL, Xu Y, Huang J, Fan HY, Jin MM. Role of phospholipase C in cytoskeleton rearrangements of dendritic cells invaded by Mycobacterium tuberculosis[J]. Journal of Zhejiang University (Medical Sciences), 2013, 42(2):184-191(in Chinese)
    [41] 夏立群,童邦卓,徐亮,苏泽杰,陈锐敏,廖保山,鲁义善.一种鰤鱼诺卡氏菌酪氨酸蛋白磷酸酶基因的克隆及功能初步研究[J].水产学报, 2017, 41(7):1017-1027 Xia LQ, Tong BZ, Xu L, Su ZJ, Chen RM, Liao BS, Lu YS. Gene cloning and preliminary function study of protein tyrosine phosphatase from Nocardia seriolae[J]. Journal of Fisheries of China, 2017, 41(7):1017-1027(in Chinese)
    [42] Fang FC. Antimicrobial reactive oxygen and nitrogen species:concepts and controversies[J]. Nature Reviews Microbiology, 2004, 2(10):820-832
    [43] Gonzalez-Carrillo C, Millan-Sauceda C, L
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ZHANG Meichao, DENG Yuting, ZHAO Fei, TAN Aiping, LUO Yuan, LI Dongming, JIANG Lan, HUANG Zhibin. Pathogenicity and whole genome analysis of a Nocardia seriolae strain isolated from snakehead[J]. Microbiology China, 2022, 49(6): 2193-2211

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  • Received:October 08,2021
  • Adopted:October 26,2021
  • Online: June 05,2022
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