Abstract
Infectious hypodermal and hematopoietic necrosis virus (IHHNV) is prevalent among farmed shrimp and results in significant reductions in shrimp production. In order to gain a better understanding of the prevalence of IHHNV in the Litopenaeus vannamei shrimp population of Shanghai, China, samples were collected during two cultivation seasons and subjected to diagnostic PCR. The results of this study showed that 167 out of 200 shrimp were positive for IHHNV, indicating a high viral prevalence (83.5 %) in farmed shrimp populations. Our results also indicated that there was a moderate correlation between IHHNV prevalence and water temperature, salinity and pH and only a slight correlation with the concentration of dissolved oxygen (DO). A mathematical model was developed in order to predict the relationship between these four characteristics of water quality and IHHNV prevalence, ultimately resulting in an estimate of the best water quality criteria (IHHNV prevalence = 0) where T = 30 °C pH = 8.0, DO = 18.3 mg/L, and salinity = 1.5 ‰. Additionally, two IHHNV genotypes were identified, the sequencing of which revealed a high similarity to the known IHHNV genotypes based on a comparison of their nucleotide and amino acid sequences. Two types of repetitive sequences were detected at both the 5′ and 3′ ends of the non-coding regions, which are commonly found in other IHHNV genomic sequences. Phylogenetic analysis indicated that the IHHNV Shanghai genotypes were closely related to strains from Ganyu and Sheyang, but not to strains originating from Fujian, China. This finding suggests that IHHNVs have emerged independently several times in China.
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Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Bell TA, Lightner DV (1984) IHHN virus: Infectivity and pathogenicity studies in Penaeus stylirostris and Penaeus vannamei. Aquaculture 38:185–194
Bonami JR, Trumper B, Mari J, Brehelin M, Lightner DV (1990) Purification and characterization of the infectious hypodermal and haematopoietic necrosis virus of penaeid shrimps. J Gen Virol 71:2657–2664
Chang PS, Chen LJ, Wang YC (1998) The effect of ultraviolet irradiation, heat, pH, ozone, salinity and chemical disinfectants on the infectivity of white spot syndrome baculovirus. Aquaculture 166:1–17
Cheng W, Chen SM, Wang FI, Hsu PI, Liu CH, Chen JC (2003) Effects of temperature, pH, salinity and ammonia on the phagocytic activity and clearance efficiency of giant freshwater prawn Macrobrachium rosenbergii to Lactococcus garvieae. Aquaculture 219:111–121
Cheng W, Wang LU, Chen JC (2005) Effect of water temperature on the immune response of white shrimp Litopenaeus vannamei to Vibrio alginolyticus. Aquaculture 250:592–601
Dhar AK, Lakshman DK, Natarajan S, Allnutt F, Van Beek NA (2007) Functional characterization of putative promoter elements from infectious hypodermal and hematopoietic necrosis virus (IHHNV) in shrimp and in insect and fish cell lines. Virus Res 127:1–8
Dhar AK, Kaizer KN, Lakshman DK (2010) Transcriptional analysis of Penaeus stylirostris densovirus genes. Virology 402:112–120
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hsieh CY, Chuang PC, Chen LC, Tu C, Chien MS, Huang KC, Kao HF, Tung MC, Tsai SS (2006) Infectious hypodermal and haematopoietic necrosis virus (IHHNV) infections in giant freshwater prawn, Macrobrachium rosenbergii. Aquaculture 258:73–79
Kalagayan H, Godin D, Kanna R, Hagino G, Sweeney J, Wyban J, Brock J (1991) IHHN Virus as an Etiological Factor in Runt-Deformity Syndrome (RDS) of Juvenile Penaeus vannamei Cultured in Hawaii. J World Aquacult Soc 22:235–243
Kim JH, Kim HK, Nguyen VG, Park BK, Choresca CH, Shin SP, Han JE, Jun JW, Park SC (2012) Genomic sequence of infectious hypodermal and hematopoietic necrosis virus (IHHNV) KLV-2010-01 originating from the first Korean outbreak in cultured Litopenaeus vannamei. Arch Virol 157:369–373
Krabsetsve K, Cullen BR, Owens L (2004) Rediscovery of the Australian strain of infectious hypodermal and haematopoietic necrosis virus. Dis Aquat Org 61:153–158
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Moullac GL, Haffner P (2000) Environmental factors affecting immune responses in Crustacea. Aquaculture 191:121–131
Lightner DV, Redman RM (1998) Shrimp diseases and current diagnostic methods. Aquaculture 164:201–220
Lightner DV, Redman RM, Bell TA, Brock JA (1983) Detection of IHHN virus in Penaeus stylirostris and P. Vannamei imported into Hawaii. J World Maric Soc 14:212–225
Lightner DV, Redman RM, Poulos BT, Nunan LM, Mari JL, Hasson KW (1997) Risk of spread of penaeid shrimp viruses in the Americas by the international movement of live and frozen shrimp. Revue scientifique et technique 16:146–160
Lo CF, Ho CH, Peng SE, Chen CH, Hsu HC, Chiu YL, Chang CF, Liu KF, Su MS, Wang CH, Kou GH (1996) White spot syndrome baculovirus (WSBV) detected in cultured and captured shrimp, crabs and other arthropods. Dis Aquat Org 27:215–225
Mari J, Bonami JR, Lightner DV (1993) Partial cloning of the genome of infectious hypodermal and haematopoietic necrosis virus, an unusual parvovirus pathogenic for penaeid shrimps; diagnosis of the disease using a specific probe. J Gen Virol 74:2637–2643
Montgomery-Brock D, Tacon AGJ, Poulos B, Lightner DV (2007) Reduced replication of infectious hypodermal and hematopoietic necrosis virus (IHHNV) in Litopenaeus vannamei held in warm water. Aquaculture 265:41–48
Nunan LM, Poulos BT, Lightner DV (2000) Use of polymerase chain reaction for the detection of infectious hypodermal and hematopoietic necrosis virus in penaeid shrimp. Mar Biotechnol 2:319–328
OIE (Office International des Epizooties) (2003) International aquatic animal health manual. Office International des Epizooties, Paris
Park JH, Lee YS, Lee S, Lee Y (1998) An infectious viral disease of penaeid shrimp newly found in Korea. Dis Aquat Org 34:71–75
Phillips MJ (1995) Shrimp culture and the environment. In: Seminar-Workshop on Aquaculture Development in Southeast Asia, Iloilo City, Philippines, 26–28 July, 1994. Aquaculture Department, Southeast Asian Fisheries Development Center (SEAFDEC/AQD), pp 37–62
Rai P, Pradeep B, Karunasagar I, Karunasagar I (2009) Detection of viruses in Penaeus monodon from India showing signs of slow growth syndrome. Aquaculture 289:231–235
Rai P, Safeena MP, Karunasagar I, Karunasagar I (2011) Complete nucleic acid sequence of Penaeus stylirostris densovirus (PstDNV) from India. Virus Res 158:37–45
Robles-Sikisaka R, Bohonak AJ, McClenaghan LR Jr, Dhar AK (2010) Genetic signature of rapid IHHNV (Infectious hypodermal and hematopoietic necrosis virus) expansion in wild Penaeus shrimp populations. PLoS One 5:e11799
Saksmerprome V, Puiprom O, Noonin C, Flegel TW (2010) Detection of infectious hypodermal and haematopoietic necrosis virus (IHHNV) in farmed Australian Penaeus monodon by PCR analysis and DNA sequencing. Aquaculture 298:190–193
Shike H, Dhar AK, Burns JC, Shimizu C, Jousset FX, Klimpel KR, Bergoin M (2000) Infectious hypodermal and hematopoietic necrosis virus of shrimp is related to mosquito brevidensoviruses. Virology 277:167–177
Stanley J, Bisaro DM, Briddon RW, Brown JK, Fauquet CM, Harrison BD, Rybicki E, Stenger DC (2005) Geminivridae: eighth report of the ICTV on virus taxonomy. In virus taxonomy—eighth report of the international committee on taxonomy of viruses. Ann Am Acad Polit Soc Sci 173:73–77
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tang KF, Poulos BT, Wang J, Redman RM, Shih HH, Lightner DV (2003) Geographic variations among infectious hypodermal and hematopoietic necrosis virus (IHHNV) isolates and characteristics of their infection. Dis Aquat Org 53:91–99
Tang KF, Lightner DV (2006) Infectious hypodermal and hematopoietic necrosis virus (IHHNV)-related sequences in the genome of the black tiger prawn Penaeus monodon from Africa and Australia. Virus Res 118:185–191
Yan Z, Lei-Butters DC, Zhang Y, Zak R, Engelhardt JF (2007) Hybrid adeno-associated virus bearing nonhomologous inverted terminal repeats enhances dual-vector reconstruction of minigenes in vivo. Human Gene Ther 18:81–87
Acknowledgments
This work was supported partially by the National Natural Science Foundation of China (41376135, 31570112), Doctoral Fund of Ministry of Education of China (20133104110006), Innovation Program of Shanghai Municipal Education Commission (14ZZ144), China, and the Special Fund for the Development of Science and Technology of Shanghai Ocean University (2015).
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C. Chai and Y. Liu contributed equally to this paper.
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Chai, C., Liu, Y., Xia, X. et al. Prevalence and genomic analysis of infectious hypodermal and hematopoietic necrosis virus (IHHNV) in Litopenaeus vannamei shrimp farmed in Shanghai, China. Arch Virol 161, 3189–3201 (2016). https://doi.org/10.1007/s00705-016-3022-5
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DOI: https://doi.org/10.1007/s00705-016-3022-5