Pathogenicity of Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease (AHPND) in shrimp (Litopanaeus vannamei) in Serang, Banten, Indonesia
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
https://orcid.org/0000-0003-0672-0685
Abstract
Abstract. Saputra A, Maftuch, Andayani S, Yanuhar U. 2023. Pathogenicity of Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease (AHPND) in shrimp (Litopanaeus vannamei) in Serang, Banten, Indonesia. Biodiversitas 24: 2365-2373. Vannamei shrimp target EMS (Early Mortality Syndrome)/AHPND (Acute Hepotopancreatic Necrosis Disease) cases in several Asian nations, including China, Vietnam, Malaysia, Thailand, India, and Indonesia. AHPND cases on shrimp farms have been reported in several Indonesian regions. The aim of this study was to evaluate the histopathological pathogenicity of Vibrio parahaemolyticus in different shrimp tissues exposed to different doses and durations of exposure. PCR amplification of V. parahaemolyticus was performed using Vp.flaE-79F (5?-GCA GCT GAT CAA AAC GTT GAG T-3?) and Vp.flaE-934R (5?-GATACCTTGTTACGACTT -3?) primers for molecular identification of bacteria isolated from shrimp exhibiting AHPND symptoms. V. parahaemolyticus positive target band at 897 bp. Bacterial isolates with green colonies on TCBS agar media were chosen for other test. Challenge tests with healthy shrimp were conducted using the V. parahaemolyticus strain. The challenge test on shrimp demonstrated the same clinical and pathological symptoms as the signs of infected shrimp in rivers, including swimming into the container’s corner and changes in the carapace’s pale color and empty midgut. The results showed that challenged shrimp displayed necrosis, atrophy, granulomas, cell sloughing, and had significantly considerable hemocyte infiltration that led to melanization. The highest percentage (63.33%) of damage was recorded in the treatment with a concentration of 108 CFU mL-1. It was also observed that virulence of V. parahaemolyticus strain varied with different concentrations. At concentrations of 108 CFU mL-1 and 106 CFU mL-1, virulence of V. parahaemolyticus strain caused 100% mortality in 73 hour post-infection (p.i). The lowest concentration limit for pathogenicity was 104 CFU mL-1 with a mortality of 48% at 73 p.i. The challenge test results showed that V. parahaemolyticus strain that causes AHPND was the main pathogen affecting vannamei shrimp in Serang, Banten, Indonesia.
##plugins.themes.bootstrap3.article.details##
References
Aguilar-Rendón KG, Lozano-Olvera R, Yáñez-Rivera B, Soto-Rodriguez SA. 2020. Bacteriological and histopathological analysis of Penaeus vannamei experimentally infected with Vibrio parahaemolyticus-AHPND strains. Diseases of Aquatic Organisms 140 (8): 167–177. DOI: 10.3354/DAO03503
Ananda RR, Sridhar R, Balachandran C, Palanisammi A, Ramesh S, Nagarajan, K. 2017. Pathogenicity profile of Vibrio parahaemolyticus in farmed Pacific white shrimp, Penaeus vannamei. Fish and Shellfish Immunology 67(3): 368–381. DOI: 10.1016/j.fsi.2017.06.020
CCAC. 2005. Canadian Council on Animal Care guidelines on: the care and use of fish in research, teaching and testing. In Canadian Council on Animal Care. 1–94pp. http://www.ccac.ca/Documents/Standards/Guidelines/Fish.pdf
Dabu IM, Lim JJ, Arabit PMT, Orense SJAB, Tabardillo JA, Corre VL, Maningas MBB. 2017. The first record of acute hepatopancreatic necrosis disease in the Philippines. Aquaculture Research 48(3): 792–799. DOI:10.1111/are.12923
Dhar AK, Piamsomboon P, Caro LFA, Kanrar S, Adami R, Juan YS. 2019. First report of acute hepatopancreatic necrosis disease (AHPND) occurring in the USA. Diseases of Aquatic Organisms 132(3): 241–247. DOI:10.3354/dao03330
Dong X, Bi D, Wang H, Zou P, Xie G, Wan X, Yang Q, Zhu Y, Chen M, Guo C, Liu Z, Wang W, Huang J. 2017. pirABvp-Bearing Vibrio parahaemolyticus and Vibrio campbellii pathogens isolated from the Same AHPND-affected pond possess highly similar pathogenic plasmids. Frontiers in Microbiology 8(8): 1–9. DOI:10.3389/fmicb.2017.01859
Dong X, Chen J, Song J, Wang H, Wang W, Ren Y, Guo C, Wang X, Tang KFJ, Huang J. 2019. Evidence of the horizontal transfer of pVA1-type plasmid from AHPND-causing V. campbellii to non-AHPND V. owensii. Aquaculture 503(12): 396–402. DOI:10.1016/j.aquaculture.2019.01.016
FAO. 2013. Report of the FAO/MARD Technical Workshop on Early Mortality Syn- drome (EMS) or Acute Hepatopancreatic Necrosis Syndrome (AHPND) of Cultured Shrimp (Under TCP/VIE/3304). In FAO Fisheries and Aquaculture Report 1053, pp 54.
FAO. 2016. The State of world fisheries and aquaculture. Contributing to Food. In Contributing to Food Security and Nutrition for All. FAO.
Feng B, Liu H, Wang M, Sun X, Pan Y. 2017. Diversity analysis of acute hepatopancreatic necrosis disease-positive Vibrio parahaemolyticus strains. Aquaculture and Fisheries 2(6): 278–285. DOI:10.1016/j.aaf.2017.10.001
Foo SM, Han W, Lee P, Gui K. 2017. crossm New Sequence Types of Vibrio aysian aquaculture pond, as revealed by whole_genome sequencing. Genome Announc 5(19): 17–19.
Fu S, Wang L, Tian H, Wei, D, Liu Y. 2018. Pathogenicity and genomic characterization of Vibrio parahaemolyticus strain PB1937 causing shrimp acute hepatopancreatic necrosis disease in China. Annals of Microbiology 68(4):175–184. DOI:10.1007/s13213-018-1328-0
Han JE, Tang KFJ, Aranguren LF, Piamsomboon P. 2017. Characterization and pathogenicity of acute hepatopancreatic necrosis disease natural mutants, pirABvp (?) V. parahaemolyticus, and pirABvp (+) V. campbellii strains. Aquaculture 470:84–90. DOI:10.1016/j.aquaculture.2016.12.022
Han JE, Lee SC, Park SC, Jeon HJ, Kim KY, Lee YS, Park S, Han SH, Kim JH, Choi S K. 2020. Molecular detection of Enterocytozoon hepatopenaei and Vibrio parahaemolyticus-associated acute hepatopancreatic necrosis disease in Southeast Asian Penaeus vannamei shrimp imported into Korea. Aquaculture 517(8):734-812. DOI:10.1016/j.aquaculture.2019.734812
Han JE, Tang KFJ, Tran LH, Lightner DV. 2015. Photorhabdus insect-related (Pir) toxin-like genes in a plasmid of Vibrio parahaemolyticus, the causative agent of acute hepatopancreatic necrosis disease (AHPND) of shrimp. Diseases of Aquatic Organisms 113(1): 33–40. DOI:10.3354/dao02830
Joshi J, Srisala J, Truong VH, Chen IT, Nuangsaeng B, Suthienkul O, Lo CF, Flegel TW, Sritunyalucksana K, Thitamadee S. 2014. Variation in Vibrio parahaemolyticus isolates from a single Thai shrimp farm experiencing an outbreak of acute hepatopancreatic necrosis disease (AHPND). Aquaculture 428(9):297–302. DOI:10.1016/j.aquaculture.2014.03.030
Kewcharoen W, Srisapoome P. 2019. Probiotic effects of Bacillus spp. from Pacific white shrimp (Litopenaeus vannamei) on water quality and shrimp growth, immune responses, and resistance to Vibrio parahaemolyticus (AHPND strains). Fish and Shellfish Immunology 94(8):175–189. DOI:10.1016/j.fsi.2019.09.013
Khimmakthong U, Sukkarun P. 2017. The spread of Vibrio parahaemolyticus in tissues of the Pacific white shrimp Litopenaeus vannamei analyzed by PCR and histopathology. Microbial Pathogenesis 113(8):107–112. DOI:10.1016/j.micpath.2017.10.028
Kumar BK, Deekshit VK, Raj JRM, Rai P, Shivanagowda BM, Karunasagar I, Karunasagar I. 2014. Diversity of Vibrio parahaemolyticus associated with disease outbreak among cultured Litopenaeus vannamei (Pacific white shrimp) in India. Aquaculture 433(11):247–251. DOI:10.1016/j.aquaculture.2014.06.016
Kumar R, Ng TH, Chang CC, Tung TC, Lin SS, Lo CF, Wang HC. 2020. Bile acid and bile acid transporters are involved in the pathogenesis of acute hepatopancreatic necrosis disease in white shrimp Litopenaeus vannamei. Cellular Microbiology 22(1):1-19. DOI:10.1111/cmi.13127
Kumar V, Nguyen DV, Baruah K, Bossier P. 2019. Probing the mechanism of VP AHPND extracellular proteins toxicity purified from Vibrio parahaemolyticus AHPND strain in germ-free Artemia test system. Aquaculture 504(8):414–419. DOI:10.1016/j.aquaculture.2019.02.029
Lai HC, Ng TH, Ando M, Lee CT, Chen IT, Chuang JC, Mavichak R, Chang SH, Yeh MD, Chiang YA, Takeyama H, Hamaguchi HO, Lo CF, Aoki T, Wang HC. 2015. Pathogenesis of acute hepatopancreatic necrosis disease (AHPND) in shrimp. Fish and Shellfish Immunology 47(2):1006–1014. DOI:10.1016/j.fsi.2015.11.008
Lazarte JMS, Kim YR, Lee JS, Chun JH, Kim SW, Jung JW, Kim J, Kayansamruaj P, Thompson KD, Kim H, Jung TS. 2021. Passive immunization with recombinant antibody vlrb-piravp /pirbvp —enriched feeds against Vibrio parahaemolyticus infection in Litopenaeus vannamei shrimp. Vaccines 9(1):1–11. DOI:10.3390/vaccines9010055
Li L, Wong HC, Nong W, Cheung MK, Law PTW, Kam KM, Kwan SS. 2014. Comparative genomic analysis of clinical and environmental strains provides insight into the pathogenicity and evolution of Vibrio parahaemolyticus. BMC Genomics 15(1): 1-2 DOI:10.1186/1471-2164-15-1135
Lim SY, Loo KW, Wong WL. 2020. Synergistic Antimicrobial Effect of a Seaweed-Probiotic Blend Against Acute Hepatopancreatic Necrosis Disease (AHPND)-Causing Vibrio parahaemolyticus. Probiotics and Antimicrobial Proteins 12(3): 906–917. DOI:10.1007/s12602-019-09616-8
Luangtrakul W, Boonchuen P, Jaree P, Kumar R, Wang HC, Somboonwiwat K. 2021. Cytotoxicity of Vibrio parahaemolyticus AHPND toxin on shrimp hemocytes, a newly identified target tissue, involves binding of toxin to aminopeptidase N1 receptor. PLoS Pathogens 17(3): 1–21. DOI:10.1371/JOURNAL.PPAT.1009463
Maralit BA, Jaree P, Boonchuen P, Tassanakajon A, Somboonwiwat K. 2018. Differentially expressed genes in hemocytes of Litopenaeus vannamei challenged with Vibrio parahaemolyticus AHPND (VPAHPND) and VPAHPND toxin. Fish and Shellfish Immunology 81(7): 284–296. DOI:10.1016/j.fsi.2018.06.054
Noble TH, Rao M, Briggs M, Shinn AP, Simon C, Wynne JW. 2021. NovacqTM improves survival of Penaeus vannamei when challenged with pathogenic Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease. Aquaculture 545(4): 737-235. DOI:10.1016/j.aquaculture.2021.737235
Nunan L, Lightner D, Pantoja C, Gomez-Jimenez S. 2014. Detection of acute hepatopancreatic necrosis disease (AHPND) in Mexico. Diseases of Aquatic Organisms : 111(1): 81–86. DOI:10.3354/dao02776
DePaola A, Kaysner CA, Bower J, Cook DW. 1998. Environmental Investigation of Vibrio parahaemolitycus in oyster after Outbreakes in Washington, Texas and New York. Applied and Environmental Microbiology 66(11): 4649 - 4654. DOI:10.1128/AEM.66.11.4649-4654.2000
Peña-Navarro N, Castro-Vásquez R, Vargas-Leitón B, Dolz G. 2020. Molecular detection of acute hepatopancreatic necrosis disease (AHPND) in Penaeus vannamei shrimps in Costa Rica. Aquaculture 523 (2):735190. DOI:10.1016/j.aquaculture.2020.735190
Rokhmani. 1994. Pengaruh Manipulasi Suhu dan Tingkat Aerasi Terhadap Infeksi Bakteri Vibrio harveyi pada Larva Udang Windu (Penaeus monodon F.). Tesis. Program Pascasarjana, Institut Pertanian Bogor. [Indonesia]
Sirikharin R, Taengchaiyaphum S, Sanguanrut P, Chi TD, Mavichak R, Proespraiwong P, Nuangsaeng B, Thitamadee S, Flegel TW, Sritunyalucksana K. 2015. Characterization and PCR detection of binary, pir-like toxins from Vibrio parahaemolyticus isolates that cause acute hepatopancreatic necrosis disease (AHPND) in shrimp. PLoS ONE 10(5): 1-16. DOI:10.1371/journal.pone.0126987
Soonthornchai W, Chaiyapechara S, Klinbunga S, Thongda W, Tangphatsornruang S, Yoocha T, Jarayabhand P, Jiravanichpaisal P. 2016. Differentially expressed transcripts in stomach of Penaeus monodon in response to AHPND infection. Developmental and Comparative Immunology 65(1): 53–63. DOI:10.1016/j.dci.2016.06.013
Soto-Rodriguez SA, Gomez-Gil B, Lozano-Olvera R, Betancourt-Lozano M, Morales-Covarrubias MS. 2015. Field and experimental evidence of Vibrio parahaemolyticus as the causative agent of acute hepatopancreatic necrosis disease of cultured shrimp (Litopenaeus vannamei) in northwestern Mexico. Applied and Environmental Microbiology 81(5): 1689–1699. DOI:10.1128/AEM.03610-14
Tarr CL, Patel JS, Puhr ND, Sowers EG, Bopp CA, Strockbine NA. 2007. Identification of Vibrio isolates by a multiplex PCR assay and rpoB sequence determination. Journal of Clinical Microbiology 45(1): 134–140. DOI:10.1128/JCM.01544-06
Theethakaew C, Nakamura S, Motooka D, Matsuda S, Kodama T, Chonsin K, Suthienkul O, Iida T. 2017. Plasmid dynamics in Vibrio parahaemolyticus strains related to shrimp Acute Hepatopancreatic Necrosis Syndrome (AHPNS). Infection, Genetics and Evolution 51(1): 211–218. DOI:10.1016/j.meegid.2017.04.007
Tinh TH, Elayaraja S, Mabrok M, Gallantiswara PCD, Vuddhakul V, Rodkhum C. 2021. Antibacterial spectrum of synthetic herbal-based polyphenols against Vibrio parahaemolyticus isolated from diseased Pacific whiteleg shrimp (Penaeus vannamei) in Thailand. Aquaculture 533(10): 1-11. DOI:10.1016/j.aquaculture.2020.736070
Tran L, Nunan L, Redman RM, Mohney LL, Pantoja CR, Fitzsimmons K, Lightner DV. 2013. Determination of the infectious nature of the agent of acute hepatopancreatic necrosis syndrome affecting penaeid shrimp. Diseases of Aquatic Organisms 105(1): 45–55. DOI:10.3354/dao02621
Trisniaty. 2015. Pengendalian Berak Putih Pada Vannamei. Trobus Aqua. [Indonesia]
Zheng Z, Wang F, Aweya JJ, Li R, Yao D, Zhong M, Li S, Zhang Y. 2018. Comparative transcriptomic analysis of shrimp hemocytes in response to acute hepatopancreas necrosis disease (AHPND) causing Vibrio parahemolyticus infection. Fish and Shellfish Immunology 74(07): 10–18. DOI:10.1016/j.fsi.2017.12.032
Most read articles by the same author(s)
- SRI ANDAYANI, M. SULAIMAN DADIONO, WIDYA TRI ELWIRA, FEBBY HADI SETYAWAN, Potency of aloe extract as immunostimulant for carp (Cyprinus carpio) against Aeromonas salmonicida , Biodiversitas Journal of Biological Diversity: Vol. 21 No. 3 (2020)
- DEVI ULINUHA, SRI ANDAYANI, ASUS MAIZAR SURYANTO HERTIKA, YUNI KILAWATI, Estimation of bacterial number in the water, sediment and biofilm of Badek and Mewek River (Malang, Indonesia) using Plate Count and eDNA Method , Biodiversitas Journal of Biological Diversity: Vol. 21 No. 8 (2020)
- NUNIK COKROWATI, YENNY RISJANI, MUHAMAD FIRDAUS, SRI ANDAYANI, Accelerated growth of Kappaphycus alvarezii using Sargassum aquifolium extract and its anatomical characteristics , Biodiversitas Journal of Biological Diversity: Vol. 22 No. 11 (2021)
- TAUFIK BUDHI PRAMONO, DIANA ARFIATI, MAHENO SRI WIDODO, UUN YANUHAR, Sexual dimorphism in morphometric characters of Mystus singaringan from Klawing River in Central Java, Indonesia: Strategic instruction for conservation development , Biodiversitas Journal of Biological Diversity: Vol. 20 No. 4 (2019)
- BUDI RIANTO WAHIDI, UUN YANUHAR, MOHAMAD MOHAMAD FADJAR, SRI ANDAYANI, Pathognomonic features and ultrastructural of Koi Herpesvirus infected Oreochromis niloticus , Biodiversitas Journal of Biological Diversity: Vol. 20 No. 2 (2019)
- VERYL HASAN, NANTASA E. ANDRAINI, WAHYU ISRONI, LUTHFIANA A. SARI, AYU L. NAFISYAH, NINA N. DEWI, DIAN N. A. PUTRI, TYAS A. B. PRASASTI, ACHMADI A. RAMADHANI, KIKI DANIEL, JOSIE SOUTH, LUCAS O. VIEIRA, FELIPE P. OTTONI, MAFTUCH, ABDUL R. FAQIH, PANDU. Y. A. P. WIRABUANA, MUHAMMAD B. TAMAM, FITRI S. VALEN, Fish diversity of the Bengawan Solo River estuary, East Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 4 (2023)
- SRI ANDAYANI, MOH. FADJAR, HENY SUPRASTYANI, AULIA RAHMAWATI, NURHALISA, VINA NUR NADIRO, The potential of bitter melon extract on cellular non-specific immunity of koi fish (Cyprinus carpio) after Aeromonas salmonicida infection , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 10 (2023)