Vibrio harveyi: một mầm bệnh nghiêm trọng của cá và động vật không xương sống trong nuôi trồng thủy sản

Marine Life Science and Technology - Tập 2 Số 3 - Trang 231-245 - 2020
Xiao‐Hua Zhang1, Xinxin He1, Brian Austin2
1MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
2Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK

Tóm tắt

Tóm tắtVibrio harveyi, thuộc họ Vibrionaceae của lớp Gammaproteobacteria, bao gồm các loài V. carchariaeV. trachuri như là những đồng nghĩa cấp bậc thấp hơn. Vi khuẩn này được công nhận là một mầm bệnh nghiêm trọng đối với cá biển và động vật không xương sống, bao gồm tôm penaeid, trong nuôi trồng thủy sản. Cá nhiễm bệnh có thể biểu hiện nhiều loại tổn thương, bao gồm tổn thương mắt/mù lòa, viêm dạ dày-ruột, hoại tử cơ, loét da, và bệnh thối đuôi. Đối với tôm, V. harveyi được xem là tác nhân nguyên nhân của bệnh vibriosis phát quang, trong đó các động vật bị ảnh hưởng phát sáng trong bóng tối. Có một tình trạng thứ hai ở tôm được gọi là Bolitas negricans, nơi mà ống tiêu hóa bị đầy với các khối cầu của mô bị bong ra. Cần nhận biết rằng các cơ chế gây bệnh của V. harveyi có thể khác nhau ở cá và tôm penaeid. Ở tôm, các cơ chế gây bệnh liên quan đến lipopolysaccharide nội độc tố và protease ngoại bào, cũng như sự tương tác với phage vi khuẩn. Ở cá, các cơ chế gây bệnh liên quan đến hemolysin ngoại bào (do các gen hemolysin lặp lại mã hóa), được xác định là một phospholipase B có thể inactivate các tế bào cá thông qua apoptosis, thông qua con đường kích hoạt caspase. V. harveyi có thể bước vào trạng thái sống nhưng không thể cấy ghép (VBNC), và việc hồi sinh các tế bào VBNC có thể là một lý do quan trọng cho việc bùng phát vibriosis trong nuôi trồng thủy sản. Các biện pháp kiểm soát dịch bệnh tập trung vào các thực phẩm bổ sung dinh dưỡng (bao gồm probiotics), các tác nhân kích thích miễn dịch không đặc hiệu, và vắc-xin, và ít hơn là kháng sinh và các hợp chất kháng vi sinh khác.

Từ khóa


Tài liệu tham khảo

Aguilera-Rivera D, Escalante-Herrera K, Gaxiola G, Prieto-Davó A, Rodríguez-Fuentes G, Guerra-Castro E, Hernández-López J, Chávez-Sánchez MC, Rodríguez-Canul R (2017) Immune response of the Pacific white shrimp, Litopenaeus vannamei, previously reared in biofloc and after an infection assay with Vibrio harveyi. J World Aquac Soc 50:119–136

Alipiah NM, Ramli NHS, Low C-F, Shamsudin MN, Yusoff FM (2016) Protective effects of sea cucumber surface-associated bacteria against Vibrio harveyi in brown-marbled grouper fingerlings. Aquacult Env Interac 8:147–155

Arijo S, Rico R, Chabrillon M, Diaz-Rosales P, Martínez-Manzanares E, Balebona MC, Toranzo AE, Moriñigo MA (2005) Effectiveness of a divalent vaccine for sole, Solea senegalensis (Kaup), against Vibrio harveyi and Photobacterium damselae subsp. piscicida. J Fish Dis 28:33–38

Arijo S, Brunt J, Chabrillón M, Díaz-Rosales P, Austin B (2008) Subcellular components of Vibrio harveyi and probiotics induce immune responses in rainbow trout, Oncorhynchus mykiss (Walbaum), against V. harveyi. J Fish Dis 31:579–590

Atujona D, Huang YC, Wang ZW, Jian JC, Cai SH (2019) Vibrio harveyi (VirB11) recombinant vaccine development against vibriosis in orange-spotted grouper (Epinephelus coioides). Aquac Res 50:2628–2634

Austin B, Austin DA (2016) Bacterial fish pathogens: disease of farmed and wild fish, 6th edn. Springer, Dordrecht, pp 499–601

Austin B, Pride AC, Rhodie GA (2003) Association of a bacteriophage with virulence in Vibrio harveyi. J Fish Dis 26:55–58

Bai F, Han Y, Chen J, Zhang X-H (2008) Disruption of quorum sensing in Vibrio harveyi by the AiiA protein of Bacillus thuringiensis. Aquaculture 274:36–40

Bai F, Sun B, Woo NYS, Zhang X-H (2010) Vibrio harveyi hemolysin induces ultrastructural changes and apoptosis in flounder (Paralichthys olivaceus) cells. Biochem Biophys Res Commun 395:70–75

Baletal FN, Gomez-Chiarri M (2016) Effect of Sargassum oligocystum hot-water extract on innate immune response and survival of summer flounder Paralichthys dentatus to Vibrio harveyi challenge. Isr J Acquacult-bamid 68:1289

Becket P, Gillan D, Lanterbecq D, Jangoux M, Rasolofonirina R, Rakotovao J, Eeckhaut I (2004) The skin ulceration disease in cultivated juveniles of Holothuria scabra (Holothuroidea, Echinodermata). Aquaculture 242:13–30

Bertone S, Gili C, Moizo A, Calegari L (1996) Vibrio carchariae associated with a chronic skin ulcer on a shark, Carcharhinus plumbeus (Nardo). J Fish Dis 19:429–434

Cano-Gomez A, Hoj L, Owens L, Andreakis N (2011) Multilocus sequence analysis provides basis for fast and reliable identification of Vibrio harveyi-related species and reveals previous misidentification of important marine pathogens. Syst Appl Microbiol 34:561–565

Cheng S, Zhang W-W, Zhang M, Sun L (2010) Evaluation of the vaccine potential of a cytotoxic protease and a protective immunogen from a pathogenic Vibrio harveyi strain. Vaccine 28:1041–1047

Chin YK, Al-saari N, Zulperi Z, Mohd-Aris A, Salleh A, Silvaraj S, MohamA LJY, Zamri-Saad M, Ina-Salwany MY (2020) Efficacy of bath vaccination with a live attenuated Vibrio harveyi against vibriosis in Asian seabass fingerling, Lates calcarifer. Aquac Res 51:389–399

Choudhury TG, Maiti B, Venugopal MN, Karunasagar I (2019) Influence of some environmental variables and addition of r-lysozyme on efficacy of Vibrio harveyi phage for therapy. J Biosci 44:8

Colwell RR, Grimes DJ (1984) Vibrio diseases of marine fish populations. Helgolander Meeresuntersuchungen 37:265–287

Company R, Sitja-Bobadilla A, Pujalte MJ, Garay E, Alvarez-Pellitero P, Perez-Sanchez J (1999) Bacterial and parasitic pathogens in cultured common dentex, Dentex dentex L. J Fish Dis 22:299–309

Crosbie PBB, Nowak BF (2004) Immune responses of barramundi, Lates calcarifer (Bloch), after administration of an experimental Vibrio harveyi bacterin by intraperitoneal injection, anal intubation and immersion. J Fish Dis 27:623–632

Deane EE, Jia A, Qu Z, Chen J-X, Zhang X-H, Woo NYS (2012) Induction of apoptosis in sea bream fibroblasts by Vibrio harveyi haemolysin and evidence for an anti-apoptotic role of heat shock protein 70. J Fish Dis 35:287–302

Diggles BK, Moss GA, Carson J, Anderson CD (2000) Luminous vibriosis in rock lobster Jasus verreauxi (Decapoda: Palinuridae) phyllosoma larvae associated with infection by Vibrio harveyi. Dis Aquat Organ 43:127–137

Dong HT, Taengphu S, Sangsuriya P, Charoensapsri W, Phiwsaiya K, Sornwatana T, Khunrae P, Rattanarojpon T, Senapin S (2017a) Recovery of Vibrio harveyi from scale drop and muscle necrosis disease in farmed barramundi, Lates calcarifer in Vietnam. Aquaculture 473:89–96

Dong X, Wang H, Zou P, Chen J, Liu Z, Wang X, Huang J (2017b) Complete genome sequence of Vibrio campbellii strain 20130629003S01 isolated from shrimp with acute hepatopancreatic necrosis disease. Gut Pathog 9:31

Dorsch M, Lane D, Stackebrandt E (1992) Towards a phylogeny of the genus Vibrio based on 16S ribosomal RNA sequences. Int J Syst Bacteriol 42:58–63

Esmaeili A, Sotoudeh E, Morshedi V, Bagher D, Dorafshan S (2019) Effects of dietary supplementation of bovine lactoferrin on antioxidant status, immune response and disease resistance of yellowfin sea bream (Acanthopagrus latus) against Vibrio harveyi. Fish Shellfish Immunol 93:917–923

Fabbro C, Celussi M, Russell H, Del Negro P (2011) Phenotypic and genetic diversity of coexisting Listonella anguillarum, Vibrio harveyi and Vibrio chagassi recovered from skin haemorrhages of diseased sand smelt, Atherina boyeri, in the Gulf of Trieste (NE Adriatic Sea). Lett Appl Microbiol 54:153–159

Farmer JJ III. Hickman-Brenner FW (1992) The genera Vibrio and Photobacterium. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd edn. Springer, New York, pp 2952–3011

Farmer JJ III, Janda JM, Brenner FW, Cameron DN, Birkhead KM (2005) Genus 1. Vibrio Pacini 1854, 411AL. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, 2nd edn. The Proteobacteria part B. The Gammaproteobacteria. Springer, New York, pp 494–546

Firmino J, Furones MD, Andree KB, Sarasquete C, Ortiz-Delgado JB, Asencio-Alcudia G, Gisbert E (2019) Contrasting outcomes of Vibrio harveyi pathogenicity in gilthead seabream, Sparus aurata and European seabass Dicentrarchus labrax. Aquaculture 511:734210

Fukasawa S, Nakamura K, Kamii A, Ohyama Y, Osumi M (1988a) Purification and properties of a proteinase from a marine luminous bacterium, Vibrio harveyi strain FLA-11. Agric Biol Chem 52:435–441

Fukasawa S, Nakamura K, Miyahira M, Kurata M (1988b) Some properties of two proteinases from a luminous bacterium, Vibrio harveyi strain FLN-108. Agric Biol Chem 52:3009–3014

Gauger EJ, Gomez-Chiarri M (2002) 16S ribosomal DNA sequencing confirms the synonymy of Vibrio harveyi and V. carchariae. Dis Aquat Org 52:39–46

Gauger E, Smolowitz R, Uhlinger K, Casey J, Gómez-Chiarri M (2006) Vibrio harveyi and other bacterial pathogens in cultured summer flounder, Paralichthys dentatus. Aquaculture 260:10–20

Geng X, Dong X-H, Tan B-P, Yang Q-H, Chi S-Y, Liu H-Y, Liu X-Q (2012) Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Aquac Nutr 18:46–55

Gomez-Gil B, Soto-Rodriquez S, Garcia-Gasca A, Roque A, Vazquez-Juarez R, Thompson FL, Swings J (2004) Molecular identification of Vibrio harveyi-related isolates associated with diseased aquatic organisms. Microbiology 150:1769–1777

Grimes DJ, Stemmler J, Hada H, May EB, Maneval D, Hetrick FM, Jones RT, Stoskopf M, Colwell RR (1984) Vibrio species associated with mortality of sharks held in captivity. Microb Ecol 10:271–282

Grimes DJ, Gruber SH, May EB (1985) Experimental infection of lemon sharks, Negaprion brevirostris (Poey), with Vibrio species. J Fish Dis 8:173–180

Gupta A, Verma G, Gupta P (2016) Growth performance, feed utilization, digestive enzyme activity, innate immunity and protection against Vibrio harveyi of freshwater prawn, Macrobrachium rosenbergii fed diets supplemented with Bacillus coagulans. Aquac Int 24:1379–1392

Haldar S, Maharajan A, Chatterjee S, Hunter SA, Chowdhury N, Hinenoya A, Asakura M, Yamasaki S (2010) Identification of Vibrio harveyi as a causative bacterium for a tail rot disease of sea bream Sparus aurata from research hatchery in Malta. Microbiol Res 165:639–648

Han JE, Tang KFJ, Aranguren LF, Piamsomboon P (2017) Characterization and pathogenicity of acute hepatopancreatic necrosis disease natural mutants, pirAB(vp) (−) V. parahaemolyticus, and pirAB(vp) (+) V. campbellii strains. Aquaculture 470:84–90

Harikrishnan R, Balasundaram C, Jawahar S, Heo M-S (2011a) Solanum nigrum enhancement of the immune response and disease resistance of tiger shrimp, Penaeus monodon against Vibrio harveyi. Aquaculture 318:67–73

Harikrishnan R, Balasundaram C, Heo M-S (2011b) Influence of diet enriched with green tea on innate humoral and cellular immune response of kelp grouper (Epinephelus bruneus) to Vibrio carchariae infection. Fish Shellfish Immunol 30:972–979

Harikrishnan R, Balasundaram C, Heo M-S (2012a) Effect of Inonotus obliquus enriched diet on hematology, immune response, and disease protection in kelp grouper, Epinephelus bruneus against Vibrio harveyi. Aquaculture 344–349:48–53

Harikrishnan R, Kim JS, Balasundaram C, Heo M-S (2012b) Protection of Vibrio harveyi infection through dietary administration of Pueraria thunbergiana in kelp grouper, Epinephelus bruneus. Aquaculture 324:27–32

Harikrishnan R, Kim J-S, Balasundaram C, Heo M-S (2012c) Vaccination effect of liposomes entrapped whole cell bacterial vaccine on immune response and disease protection in Epinephelus bruneus against Vibrio harveyi. Aquaculture 342:69–74

Harikrishnan R, Kim J-S, Kim M-C, Balasundaram C, Heo M-S (2012d) Zanthoxylum piperitum supplemented diet enhances disease resistance in Epinephelus bruneus against Vibrio carchariae. Fish Pathol 47:27–29

Harries LJ, Owens L (1999) Production of exotoxins by two luminous Vibrio harveyi strains known to be primary pathogens of Penaeus monodon larvae. Dis Aquat Org 38:11–22

Henke JM, Bassler BL (2004) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186:3794–3805

Hispano C, Nebra Y, Blanch AR (1997) Isolation of Vibrio harveyi from an ocular lesion in the short sunfish (Mola mola). Bull Eur Assoc Fish Pathol 17:104–107

Hoffmann M, Monday SR, Fischer M, Brown EW (2012) Genetic and phylogenetic evidence for misidentification of Vibrio species within the Harveyi clade. Lett Appl Microbiol 54:160–165

Hu Y-H, Sun L (2011) A bivalent Vibrio harveyi DNA vaccine induces strong protection in Japanese flounder (Paralichthys olivaceus). Vaccine 29:4328–4333

Hu Y-H, Cheng S, Zhang M, Sun L (2011) Construction and evaluation of a live vaccine against Edwardsiella tarda and Vibrio harveyi: laboratory vs. mock field trial. Vaccine 29:4081–4085

Huang ZJ, Tang JJ, Li M, Fu YC, Dong CF, Zhong JF, He JG (2012) Immunological evaluation of Vibrio alginolyticus, Vibrio harveyi, Vibrio vulnificus and infectious spleen and kidney necrosis virus (ISKNV) combined-vaccine efficacy in Epinephelus coioides. Vet Immunol Immunopathol 150:61–68

Ishimaru K, Muroga K (1997) Taxonomical re-evaluation of two pathogenic Vibrio species isolated from milkfish and swimming crab. Fish Pathol 32:59–64

Iwamoto Y, Suzuki Y, Kurita A, Watanabe Y, Shimizu T, Ohgami H, Yanagihara Y (1995) Vibrio trachuri sp. nov., a new species isolated from diseased Japanese horse mackerel. Microbiol Immunol 39:831–837

Jin G, Wang S, Yu M, Yan S, Zhang X-H (2010) Identification of a marine antagonistic strain JG1 and establishment of a polymerase chain reaction detection technique based on the gyrB gene. Aquac Res 41:1867–1874

Johnson FH, Shunk IV (1936) An interesting new species of luminous bacteria. J Bacteriol 31:585–592

Kannappan S, Sivakumar K, Sethi S (2018) Protective effect of mangrove (Rhizophora apiculata) leaves extract in shrimp (Penaeus monodon) larvae against bio-luminescent disease-causing Vibrio harveyi bacteria. Span J Agric Res 16:e0501

Karunasagar I, Pai R, Malathi GR, Karunasagar I (1994) Mass mortality of Penaeus monodon larvae due to antibiotic-resistant Vibrio harveyi infection. Aquaculture 128:203–209

Ke H-M, Prachumwat A, Yu C-P, Yang Y-T, Promsri S, Liu K-F, Lo C-F, Lu M-YJ, Lai M-C, Tsai IJ, Li W-H (2017) Comparative genomics of Vibrio campbellii strains and core species of the Vibrio harveyi clade. Sci Rep 7:41394

Khemayan K, Pasharawipas T, Puiprom O, Sriurairatana S, Suthienkul O, Flegel TW (2006) Unstable lysogeny and pseudolysogeny in Vibrio harveyi siphovirus-like phage 1. Appl Environ Microbiol 72:1355–1363

Kim J-S, Harikrishnan R, Kim M-C, Jang I-S, Kim D-H, Hong S-H, Balasundaram C, Heo M-S (2011) Enhancement of Eriobotrya japonica extracts on non-specific immune response and disease resistance in kelp grouper Epinephelus bruneus against Vibrio carchariae. Fish Shellfish Immunol 31:1193–1200

Kraxberger-Beatty T, McGarey DJ, Grier HJ, Lim DV (1990) Vibrio harveyi, an opportunistic pathogen of common snook, Centropomus undecimalis (Block), held in captivity. J Fish Dis 13:557–560

Lal TM, Sano M, Ransangan J (2017) Isolation and characterization of large marine bacteriophage (Myoviridae), VhKM4 infecting Vibrio harveyi. J Aquat Anim Health 29:26–30

Lee CA (1996) Pathogenicity islands and the evolution of bacterial pathogens. Infect Agents Dis 5:1–7

Lee J-H, Kim J-W, Kang W-J, Ko D-W, Kim J-M, Choi S-H, Park K-H (2018) Effects of beta-1,3-glucan on innate immunity responses and mortality induced by Vibrio harveyi, hemorrhagic septicemia virus, or Miamiensis avidus in the olive flounder Paralichthys olivaceus. Aquac Int 26:743–756

Lee KK, Liu PC, Kou GH, Chen SN (1997) Investigation on the major exotoxin of Vibrio harveyi 770527 isolated from diseased Penaeus monodon. Rep Fish Dis Res 18:33–42

Lee KK, Liu PC, Chuang WH (2002) Pathogenesis of gastroenteritis caused by Vibrio carchariae in cultured marine fish. Mar Biotechnol 4:267–277

Li H, Xiao J, Zhou Y, Wang Q, Zhang Y (2017) Sensitivity improvement of rapid Vibrio harveyi detection with an enhanced chemiluminescent-based dot blot. Lett Appl Microbiol 65:206–212

Li M-F, Wang C-L, Sun L (2011) A pathogenic Vibrio harveyi lineage causes recurrent disease outbreaks in cultured Japanese flounder (Paralichthys olivaceus) and induces apoptosis in host cells. Aquaculture 319:30–36

Lin H, Yu M, Wang X, Zhang X-H (2018) Comparative genomic analysis reveals the evolution and environmental adaptation strategies of vibrios. BMC Genomics 19:135

Liu L, Ge M, Zheng X, Tao Z, Zhou S, Wang G (2016) Investigation of Vibrio alginolyticus, V. harveyi and V. parahaemolyticus in large yellow croaker, Pseudosciaena crocea (Richardson) reared in Xiangshan Bay. China Aquac Rep 3:220–224

Liu PC, Lee KK, Chen SN (1996) Pathogenicity of different isolates of Vibrio harveyi in tiger prawn, Penaeus monodon. Lett Appl Microbiol 22:413–416

Liu PC, Lee KK, Tu CC, Chen SN (1997) Purification and characterization of a cysteine protease produced by pathogenic luminous Vibrio harveyi. Curr Microbiol 35:32–39

Liu P-C, Chuang W-H, Lee K-K (2003) Infectious gastroenteritis caused by Vibrio harveyi (V. carchariae) in cultured red drum (Sciaenops ocellatus). J Appl Ichthyol 19:59–61

Mao Z, He C, Qiu Y, Chen J (2011) Expression of Vibrio harveyi ompK in the yeast Pichia pastoris: the first step in developing an oral vaccine against vibriosis? Aquaculture 318:268–272

Mohamad N, Roseli FAM, Azmai MNA, Saad MZ, Yasin ISM, Zulkiply NA, Nasruddin NS (2019) Natural concurrent infection of Vibrio harveyi and V. alginolyticus in cultured hybrid groupers in Malaysia. J Aquat Anim Health 31:88–96

Mohd-Aris A, Saad MZ, Daud HM, Yusof MT, Ina-Salwany MY (2019) Vibrio harveyi protease deletion mutant as a live attenuated vaccine candidate against vibriosis and transcriptome profiling following vaccination for Epinephelus fuscoguttatus. Aquac Int 27:125–140

Mohi MM, Kuratani M, Miyazaki T, Yoshida T (2010) Histopathological studies of Vibrio harveyi—sinfected tiger puffer, Takifugu rubripes (Temminck et Schlegel), cultured in Japan. J Fish Dis 33:833–840

Montero AB, Austin B (1999) Characterization of extracellular products from an isolate of Vibrio harveyi recovered from diseased post-larval Penaeus vannamei (Bonne). J Fish Dis 22:377–386

Montgomery MT, Kirchman DL (1993) Role of chitin binding proteins in the specific attachment of the marine bacterium Vibrio harveyi to chitin. Appl Environ Microbiol 59:373–379

Montgomery MT, Kirchman DL (1994) Induction of chitin-binding proteins during the specific attachment of the marine bacterium Vibrio harveyi to chitin. Appl Environ Microbiol 60:4284–4288

Munro J, Oakey J, Bromage E, Owens L (2003) Experimental bacteriophage-mediated virulence in strains of Vibrio harveyi. Dis Aquat Organ 54:187–194

Muthukrishnan S, Defoirdt T, Ina-Salwany MY, Yusoff FM, Shariff M, Ismail SI, Natrah I (2019) Vibrio parahaemolyticus and Vibrio harveyi causing Acute Hepatopancreatic Necrosis Disease (AHPND) in Penaeus vannamei (Boone, 1931) isolated from Malaysian shrimp ponds. Aquaculture 511:734227

Nakayama T, Nomura N, Matsumura M (2005) Analysis of the relationship between luminescence and toxicity of Vibrio carchariae pathogenic to shrimp. Fish Sci 71:1236–1242

Nguyen HT, Nguyen TTT, Wang T, Wang C, Chen C (2017) Effectiveness of formalin-killed vaccines containing CpG oligodeoxynucleotide 1668 adjuvants against Vibrio harveyi in orange-spotted grouper. Fish Shellfish Immunol 68:124–131

Nguyen HT, Nguyen TTT, Chen Y-C, Vu-Khac H, Wang P-C, Chen S-C (2018) Enhanced immune responses and effectiveness of refined outer membrane protein vaccines against Vibrio harveyi in orange-spotted grouper (Epinephelus coioides). J Fish Dis 41:1349–1358

Nishibuchi M, Kaper JB (1985) Nucleotide sequence of the thermostable direct hemolysin gene of Vibrio parahaemolyticus. J Bacteriol 162:558–564

Nishimori E, Hasegawa O, Numata T, Wakabayashi H (1998) Vibrio carchariae causes mass mortalities in Japanese abalone, Sulculus diversicolor supratexta. Fish Pathol 33:495–502

Oakey HJ, Owens L (2000) A new bacteriophage, VHML, isolated from a toxin-producing strain of Vibrio harveyi in tropical Australia. J Appl Microbiol 89:702–709

Oakey HJ, Cullen BR, Owens L (2002) The complete nucleotide sequence of the Vibrio harveyi bacteriophage VHML. J Appl Microbiol 93:1089–1098

Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425

Owens L, Austin DA, Austin B (1996) Effect of siderophore production in Vibrio harveyi isolates. Dis Aquat Organ 27:157–160

Pang H-Y, Li Y, Wu Z-H, Jian J-C, Lu Y-S, Cai S-H (2010) Immunoproteomic analysis and identification of novel immunogenic proteins from Vibrio harveyi. J Appl Microbiol 109:1800–1809

Pang JH, Wang Q, Fei YJ, Zhua P, Qiao LL, Huang HL, Dang CY, Gao WF (2019) A real-time recombinase polymerase amplification assay for the rapid detection of Vibrio harveyi. Mol Cell Probes 44:8–13

Pang L, Zhang X-H, Zhong Y, Chen J, Li Y, Austin B (2006) Identification of Vibrio harveyi using PCR amplification of the toxR gene. Lett Appl Microbiol 43:249–255

Pasharawipas T, Thaikua S, Sriurairatana S, Ruangpan L, Direkbusarakum S, Manopvisetcharean J, Flegel TW (2005) Partial characterization of a novel bacteriophage of Vibrio harveyi isolated from shrimp culture ponds in Thailand. Virus Res 114:63–69

Pavia AT, Bryan JA, Maher KL, Hester TR, Farmer JJ (1989) Vibrio carchariae infection after a shark bite. Ann Intern Med 111:85–86

Pedersen K, Verdonck L, Austin B, Austin DA, Blanch AR, Grimont PAD, Jofre J, Koblavi S, Larsen JL, Tiainen T, Vigneulle M, Swings J (1998) Taxonomic evidence that Vibrio carchariae Grimes et al 1985 is a junior synonym of Vibrio harveyi (Johnson and Shunk 1936) Baumann et al. 1981. Int J Syst Bacteriol 48:749–758

Pinto MF, Baptista T, Afonso TTN (2017) Development of a new multiplex-PCR tool for the simultaneous detection of the fish pathogens Vibrio alginolyticus, Vibrio anguillarum, Vibrio harveyi and Edwardsiella tarda. Aquat Living Res 30:4

Prasad S, Morris PC, Hansen R, Meaden PG, Austin B (2005) A novel bacteriocin-like substance (BLIS) from a pathogenic strain of Vibrio harveyi. Microbiology 151:3051–3058

Prayitno SB, Latchford JW (1995) Experimental infections of crustaceans with luminous bacteria related to Photobacterium and Vibrio—effect of salinity and pH on infectiosity. Aquaculture 132:105–112

Pujalte MJ, Sitjá-Bobadilla A, Macián MC, Belloch C, Álvarez-Pellitero P, Pérez-Sánchez J, Uruburu F, Garay E (2003) Virulence and molecular typing of Vibrio harveyi strains isolated from cultured dentex, gilthead sea bream and European sea bass. Syst Appl Microbiol 26:284–292

Qin G, Wang X, Tan S, Lin Q (2017) A bacterial infection by Vibrio harveyi causing heavy reduction of cultured lined seahorse Hippocampus erectus. J Fish Dis 40:601–605

Qin YX, Wang J, Su YQ, Wang DX, Chen XZ (2006) Studies on the pathogenic bacterium of ulcer disease in Epinephelus awoara. Acta Oceanol Sin 25:154–159

Raj ST, Lipton AP, Chauhan GS (2010) Characterization and infectivity evaluation of Vibrio harveyi causing white patch disease among captive reared seahorses, Hippocampus kuda. Indian J Mar Sci 39:151–156

Ransangan J, Mustafa S (2009) Identification of Vibrio harveyi isolated from diseased Asian sea bass Lates calcarifer by use of 16S ribosomal DNA sequencing. J Aquat Anim Health 21:150–155

Restrepo L, Bayot B, Arciniegas S, Bajana L, Betancourt I, Panchana F, Munoz AR (2018) PirVP genes causing AHPND identified in a new Vibrio species (Vibrio punensis) within the commensal Orientalis clade. Sci Rep 8:13080

Robertson PAW, Caldero J, Carrera L, Stark JR, Zherdmant M, Austin B (1998) Experimental Vibrio harveyi infections in Penaeus vannamei larvae. Dis Aquat Organ 32:151–155

Ruangpan L, Danayadol Y, Direkbusarakom S, Siurairatana S, Flegel TW (1999) Lethal toxicity of Vibrio harveyi to cultivated Penaeus monodon induced by a bacteriophage. Dis Aquat Organ 35:195–201

Saeed MO (1995) Association of Vibrio harveyi with mortalities in cultured marine fish in Kuwait. Aquaculture 136:21–29

Schaeck M, Duchateau L, Van den Broeck W, Van Trappen S, De Vos P, Coulombet C, Boon N, Haesebrouck F, Decostere A (2016) Vibrio lentus protects gnotobiotic sea bass (Dicentrarchus labrax L.) larvae against challenge with Vibrio harveyi. Vet Microbiol 185:41–48

Selvin J, Huxley AJ, Lipton AP (2005) Pathogenicity, antibiogram and biochemical characteristics of luminescent Vibrio harveyi associated with 'Black Shell Disease’ of Penaeus monodon. Fish Technol 42:191–196

Shen GM, Shi CY, Fan C, Jia D, Wang SQ, Xie GS, Li GY, Mo ZL, Huang J (2017) Isolation, identification and pathogenicity of Vibrio harveyi, the causal agent of skin ulcer disease in juvenile hybrid groupers Epinephelus fuscoguttatus x Epinephelus lanceolatus. J Fish Dis 40:1351–1362

Soffientino B, Gwaltney T, Nelson DR, Specker JL, Mauel M, Gomez-Chiarri M (1999) Infectious necrotizing enteritis and mortality caused by Vibrio carchariae in summer flounder Paralichthys dentatus during intensive culture. Dis Aquat Org 38:201–210

Soto-Rodriguez SA, Roque A, Lizarraga-Partida ML, Guerra-Flores AL, Gomez-Gil B (2003) Virulence of luminous vibrios to Artemia franciscana nauplii. Dis Aquat Organ 53:231–240

Stalin N, Srinivasan P (2017) Efficacy of potential phage cocktails against Vibrio harveyi and closely related Vibrio species isolated from shrimp aquaculture environment in the south east coast of India. Vet Microbiol 207:83–96

Sun BG, Zhang X-H, Tang XX, Wang SS, Zhong YB, Chen JX, Austin B (2007) A single residue change in Vibrio harvei hemolysin results in the loss of phospholipase and haemolytic activities and pathogenicity for turbot (Scophthalmus maximus). J Bacteriol 189:2575–2579

Sun F, Chen J, Zhong L, Zhang X-H, Wang R, Guo Q, Dong Y (2008) Characterization and virulence retention of viable but nonculturable cells. FEMS Microbiol Ecol 64:37–44

Sun K, Hu Y-H, Zhang X-H, Bai F-F, Sun L (2009) Identification of vhhP2, a novel genetic marker of Vibrio harveyi, and its application in the quick detection of V. harveyi from animal specimens and environmental samples. J Appl Microbiol 107:1251–1257

Talpur AD, Ikhwanuddin M (2012) Dietary effects of garlic (Allium sativum) on haemato-immunological parameters, survival, growth, and disease resistance against Vibrio harveyi infection in Asian sea bass, Lates calcarifer (Bloch). Aquaculture 364:6–12

Tan XH, Sun ZZ, Huang Z, Zhou CP, Lin HZ, Tan LJ, Xun PW, Huang Q (2017) Effects of dietary hawthorn extract on growth performance, immune responses, growt- and immune-related genes expression of juvenile golden pompano (Trachinotus ovatus) and its susceptibility to Vibrio harveyi infection. Fish Shellfish Immunol 70:656–664

Thompson FL, Hoste B, Vandemeulebroecke K, Engelbeen K, Denys R, Swings J (2002) Vibrio trachuri Iwamoto et al. 1995 is a junior synonym of Vibrio harveyi (Johnson and Shunk 1936) Baumann et al. 1981. Int J Syst Evol Microbiol 52: 973–976

Thompson FL, Gomez-Gil B, Vasconcelos ATR, Sawabe T (2007) Multilocus sequence analysis reveals that Vibrio harveyi and V. campbellii are distinct species. Appl Environ Microbiol 73:4279–4285

Urbanczyk H, Ogura Y, Hayashi T (2013) Taxonomic revision of Harveyi clade bacteria (family Vibrionaceae) based on analysis of whole genome sequences. Int J Syst Evol Microbiol 63:2742–2751

Verma VK, Rani KV, Kumar SR, Prakash O (2018) Leucaena leucocephala pod seed protein as an alternative to animal protein in fish feed and evaluation of its role to fight against infection caused by Vibrio harveyi and Pseudomonas aeruginosa. Fish Shellfish Immunol 76:324–332

Vidgen M, Carson J, Higgins M, Owens L (2006) Changes to the phenotypic profile of Vibrio harveyi myovirus-like (VHML) bacteriophage. J Appl Microbiol 100:481–487

Wang B-K, Yu J-H, Li Y, Ji W-S, Xu H-S (2002) Isolation and identification of pathogen (Vibrio harveyi) from sea pearch, Lateolabrax japonicus. J Fishery Sci 9:52–55 (in Chinese, abstract in English)

Wang C, Zhang X-H, Jia A, Chen J, Austin B (2008) Identification of immune-related genes from kidney and spleen of turbot, Psetta maxima (L.), by suppression subtractive hybridization following challenge with Vibrio harveyi. J Fish Dis 31:505–514

Wang HY, Zhu F, Huang YC, Ding Y, Jian JC, Wu ZH (2017) Construction of glutathione peroxidase (GPx) DNA vaccine and its protective efficiency on the orange-spotted grouper (Epinephelus coioides) challenged with Vibrio harveyi. Fish Shellfish Immunol 60:529–536

Wang Q, Chen J, Liu R, Jia J (2011) Identification and evaluation of an outer membrane protein OmpU from a pathogenic Vibrio harveyi isolate as vaccine candidate in turbot (Scophthalmus maximus). Lett Appl Microbiol 53:22–29

Wang RX, Yao T, Liu XJ, Wang JY (2018) Isolation and characterisation of Vibrio harveyi as etiological agent of foot pustule disease in the abalone Haliotis discus hannai Ino 1953. Indian J Fish 65:79–85

Won KM, Park S (2008) Pathogenicity of Vibrio harveyi to cultured marine fishes in Korea. Aquaculture 285:8–13

Xiao J, Liu L, Ke Y, Li X, Liu Y, Pan Y, Yan S, Wang Y (2017) Shrimp AHPND-causing plasmids encoding the PirAB toxins as mediated by pirAB-Tn903 are prevalent in various Vibrio species. Sci Rep 7:42177

Xu H-S, Roberts N, Singleton FL, Attwell RW, Grimes DJ, Colwell R (1982) Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol 8:313–323

Xu XD, Lui KF, Wang SF, Guo WL, Xie ZY, Zhou YC (2017) Identification of pathogenicity, investigation of virulent gene distribution and development of a virulent strain-specific detection PCR method for Vibrio harveyi isolated from Hainan province and Guangdong province, China. Aquaculture 468:226–234

Xu WT, Jiao CL, Bao PC, Liu Q, Wang PB, Zhang RL, Liu XH, Zhang YX (2019) Efficacy of Montanide (TM) ISA 763 A VG as aquatic adjuvant administrated with an inactivated Vibrio harveyi vaccine in turbot (Scophthalmus maximus L.). Fish Shellfish Immunol 84:56–61

Yang Q, Han Y, Zhang X-H (2011) Detection of quorum-sensing signal molecules in the family Vibrionaceae. J Appl Microbiol 110:1438–1448

Yii K-C, Yang TI, Lee K-K (1997) Isolation and characterization of Vibrio carchariae, a causative agent of gastroenteritis in the groupers, Epinephelus coioides. Curr Microbiol 35:109–115

Yu M, Wang J, Tang K, Shi X, Wang S, Zhu W-M, Zhang X-H (2012) Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology-SGM 158:835–842

Zhang C, Yu L, Qian R (2008) Cloning and expression of Vibrio harveyi OmpK* and GAPDH* genes and their potential application as vaccines in large yellow croakers Pseudosciaena crocea. J Aquat Anim Health 20:1–11

Zhang X-H (2001) Studies on the pathogenicity mechanisms of the fish pathogen Vibrio harveyi. PhD thesis, Heriot-Watt University, UK.

Zhang X-H, Austin B (2000) Pathogenicity of Vibrio harveyi to salmonids. J Fish Dis 23:93–102

Zhang X-H, Lin H, Wang X, Austin B (2018) Significance of Vibrio species in the marine organic carbon cycle—a review. Sci China Earth Sci 61:1357–1368

Zhang X-H, Meaden PG, Austin B (2001) Duplication of hemolysin genes in a virulent isolate of Vibrio harveyi. Appl Environ Microbiol 67:3161–3167

Zhong Y, Zhang X-H, Chen J, Chi Z, Sun B, Li Y, Austin B (2006) Overexpression, characterization, and pathogenicity of Vibrio harveyi hemolysin VHH. Infect Immun 74:6001–6005

Zhou CP, Lin HZ, Xia DM, Yang K, Yang YY, Huang Z, Wei Y (2016) Effect of dietary marine red yeast Rhodotorula mucilaginosa on the growth performance, and also non-specific immune responses of juvenile golden pompano Trachinotus ovatus when challenged with Vibrio harveyi. Israeli J Aquacult—BAMIDGEH 68: 1262

Zhou J, Fang W, Yang X, Zhou S, Hu L, Li X, Qi X, Su H, Xie L (2012) A nonluminescent and highly virulent Vibrio harveyi strain is associated with ‘‘Bacterial White Tail Disease’’ of Litopenaeus vannamei shrimp. PLoS ONE 7:e29961

Zhu K, Chi Z, Li J, Zhang F, Li M, Yasoda HN, Wu L (2006) The surface display of haemolysin from Vibrio harveyi on yeast cells and their potential applications as live vaccines in marine fish. Vaccine 24:6046–6052

Zhu ZM, Dong CF, Weng SP, He JG (2018) The high prevalence of pathogenic Vibrio harveyi with multiple antibiotic resistance in scale drop and muscle necrosis disease of the hybrid grouper, Epinephelus fuscoguttatus (♀) x E. lanceolatus (♂), in China. J Fish Dis 41:589–601

Zhu ZM, Dong CF, Weng SP, He JG (2019) Identification of outer membrane protein To1C as the major adhesin and potential vaccine candidate for Vibrio harveyi in hybrid grouper, Epinephelus fuscoguttatus (female) x E-lanceolatus (male). Fish Shellfish Immunol 86:143–151

Zorrilla I, Arijo S, Chabrillon M, Diaz P, Martinez-Manzanares E, Balebona MC, Morinigo MA (2003) Vibrio species isolated from diseased farmed sole, Solea senegalensis (Kaup), and evaluation of the potential virulence role of their extracellular products. J Fish Dis 26:103–108