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The Effect of Immersion Duration of Zoothamnium penaei Crude Protein Extracts to Stimulate Immune System in Litopenaeus vannamei Against Enterocytozoon hepatopenaei (EHP)
Corresponding Author(s) : Gunanti Mahasri
Jurnal Ilmiah Perikanan dan Kelautan, Vol. 15 No. 2 (2023): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Highlight Research
- The effect of immersion duration of shrimp to the immunostimulant from crude protein Zoothamnium penaei was determined.
- 20-minute immersion duration in crude protein from Zoothamnium penaei was found to increase the phagocytosis activities, phenoloxidase, and improve hepatopancreases of the shrimp.
- There is increase in phagocytosis activities, phenoloxidase and improved hepatopancreases cell within a three-week maintenance of shrimp with immersion after each seven days.
- There is interaction between immersion duration and maintenance time of shrimp into the crude protein from Zoothamnium penaei.
Abstract
Enterocytozoon hepatopenaei (EHP) is a spore-forming microsporidia intracellular parasite, which slough off the cells of the hepatopancreases of the shrimp. This study was intended to determine the effect of immersion duration and maintenance time to stimulate the immune system of shrimps by using a crude protein from Zoothamnium penaei to protect against EHP infections. The study used a completely randomized design where shrimps were divided into four groups each having five replicates. Groups P1, P2, P3 were immersed in immunostimulant for 10, 15, and 20 minutes respectively, except negative control. The phenoloxidase, phagocytosis activities, histopathology study were determined. Also, the molecular diagnosis of EHP was measured to confirm EHP infection in the shrimp samplesThe phenoloxidase activity significantly increased after immersion for 20 minutes (P3) from 0.64-, 0.72-, and 0.78-units min-1 mil -1 of protein on the first week, second week and third week, respectively. The phagocytosis activities of the sample immersed for 20 minutes were significantly increased to 68% on the second week. The sample also showed improved hepatopancreases epithelial cells with only 26% necrotic cell, less EHP spore and vacuolation. There was an interaction between immersion duration and maintenance time of the L. vannamei immersed in crude protein from Zoothamnium penaei. Twenty minutes immersion were significantly found to stimulate the immune system of the shrimp against EHP. The present work revealed that, the application of crude protein from Z. penaei is effective against EHP in shrimp culture.
Keywords
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- Apines-Amar, M. J. S., & Amar, E. C. (2015). Use of immunostimulants in shrimp culture: An update. In C. M. A. Caipang, M. B. I. Bacano-Maningas, & F. F. Fagutao (Ed.), Biotechnological advances in shrimp health management in the Philippines. (pp. 45-71). Kerala, India: Research Signpost.
- Aranguren, L. F., Han, J. E., & Tang, K. F. J. (2017). Enterocytozoon hepatopenaei (EHP) is a risk factor for acute hepatopancreatic necrosis disease (AHPND) and septic hepatopancreatic necrosis (SHPN) in the Pacific white shrimp Penaeus vannamei. Aquaculture, 471:37-42.
- Babu, D. T., Antony, S. P., Joseph, S. P., Bright, A. R., & Philip, R. (2013). Marine yeast Candida aquaetextoris S527 as a potential immunostimulant in black tiger shrimp Penaeus monodon. Journal of Invertebrate Pathology, 112(3):243-252.
- Bairwa, M. K., Jakhar, J. K., Satyanarayana, Y., & Reddy, A. D. (2012). Animal and plant originated immunostimulants used in aquaculture. Journal of Natural Product and Plant Resources, 2(3):397-400.
- Barman, D., Nen, P., Mandal, S. C., & Kumar, V. (2013). Immunostimulants for aquaculture health management. Journal of Marine Science: Research & Development, 03(03).
- Caro, L. F. A., Mai, H. N., Pichardo, O., Cruz-Flores, R., Hanggono, B., & Dhar, A. K. (2020). Evidences supporting Enterocytozoon hepatopenaei association with white feces syndrome in farmed Penaeus vannamei in Venezuela and Indonesia. Diseases of Aquatic Organisms, 141:71–78.
- Citarasu, T., Sivaram, V., Immanuel, G., Rout, N., & Murugan, V. (2006). Influence of selected Indian immunostimulant herbs against white spot syndrome virus (WSSV) infection in black tiger shrimp, Penaeus monodon with reference to haematological, biochemical and immunological changes. Fish and Shellfish Immunology, 21(4):372-384.
- Declarador, R. S., Serrano Jr, A. E., & Corre Jr, V. L. (2014). Ulvan extract acts as immunostimulant against white spot syndrome virus (WSSV) in juvenile black tiger shrimp Penaeus monodon. AACL Bioflux, 7(3):153-161.
- Desrina, Prayitno, B. B., Haditomo, A. H. C., Latritiani, R., & Sarjito, S. (2020). Detection of Enterocytozoon hepatopenaei (EHP) DNA in the polychaetes from shrimp ponds suffering white feces syndrome outbreaks. Biodiversitas, 21(1):369-374.
- Flores-Miranda, M. del C., Luna-González, A., Campa-Córdova, Á. I., González-Ocampo, H. A., Fierro-Coronado, J. A., & Partida-Arangure, B. O. (2011). Microbial immunostimulants reduce mortality in whiteleg shrimp (Litopenaeus vannamei) challenged with Vibrio sinaloensis strains. Aquaculture, 320(1-2):51-55.
- Fu, Y. W., Hou, W. Y., Yeh, S. T., Li, C. H., & Chen, J. C. (2007). The immunostimulatory effects of hot-water extract of Gelidium amansii via immersion, injection and dietary administrations on white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish & Shellfish Immunology, 22(6):673-685.
- Ganguly, S., Paul, I., & Mukhopadhayay, S. K. (2010). Application and effectiveness of immunostimulants, probiotics, and prebiotics in aquaculture: A review. The Israeli Journal of Aquaculture - Bamidgeh, 62(3):130-138.
- Harijanto. (2012). Kemampuan proteksi imunostimulan dari protein membran imunogenik Zoothamnium penaei terhadap Zoothamniosis pada udang vanname (Litopenaeus vannamei). Thesis. Surabaya: Universitas Airlangga.
- Hernroth, B., Sköld, H. N., Wiklander, K., Jutfelt, F., & Baden, S. (2012). Simulated climate change causes immune suppression and protein damage in the crustacean Nephrops norvegicus. Fish & Shellfish Immunology, 33(5):1095-1101.
- Hidayat, R. P. (2017). Evaluasi pemberian crude protein Zoothamnium penaei Terhadap laju pertumbuhan, respon imun dan kelulushidupan udang vaname (Litopenaeus vannamei) di tambak. Jurnal Biosains Pascasarjana, 19(2):111-132.
- Huang, X., Zhou, H., & Zhang, H. (2006). The effect of Sargassum fusiforme polysaccharide extracts on vibriosis resistance and immune activity of the shrimp, Fenneropenaeus chinensis. Fish & Shellfish Immunology, 20(5):750-757.
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- Lowry, Br O. H., Rosebrough, N. J., Farr, A, L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1):265-275.
- Maftuch, Prasetio, E., Sudianto, A., Rozik, M., Nurdiyani, R., Sanusi, E., Nursyam, H., Fariedah, F., Marsoedi, & Murachman. (2013). Improvement of innate immune responses and defense activity in tiger shrimp (Penaeus monodon Fab.) by intramuscular administration of the outer membrane protein Vibrio alginolyticus. SpringerPlus, 2(1):1-8.
- Mahasri, G., Kusdarwati, R., Kismiyati, Rozi, & Gustrifandi, H. (2018). Effectivity of immunostimulant from Zoothamnium penaei protein membrane for decreasing the mortality rate of white shrimp (Litopenaeus vannamei) in traditional plus pond. IOP Conference Series: Earth and Environmental Science, 137(1).
- Mai, H. N., Cruz-Flores, R., Caro, L. F. A., White, B. N., & Dhar, A. K. (2020). A comparative study of Enterocytozoon hepatopenaei (EHP) challenge methods in Penaeus vannamei. Journal of Invertebrate Pathology, 171:107336.
- Marimuthu, S., Raju, C. S., & Bhassu, S. (2021). Clinical Investigation and molecular diagnosis of microsporidian Enterocytozoon hepatopenaei (EHP) in shrimps from Selangor, Malaysia. 5(2):67-75.
- Marwiyah, U. C., Mahasri, G., Ratnasari, R. E., & Wiradana, P. A. (2019). Total plate count and identification of vibrio in pacific white shrimp (Litophenaeus vannamei) from ponds and in those exposed to immunogenic protein membrane Zoothamnium penaei. IOP Conference Series: Earth and Environmental Science, 236(1):012087.
- Mohan, K., Ravichandran, S., Muralisankar, T., Uthayakumar, V., Chandirasekar, R., Seedevi, P., & Rajan, D. K. (2019). Potential uses of fungal polysaccharides as immunostimulants in fish and shrimp aquaculture: A review. Aquaculture, 500:250-263.
- Nkuba, A., Gunanti, M., Nunuk, D. R. L., & Adamu Ayubu, M. (2021). Correlation of Nitrite and Ammonia Concentration with Prevalence of. Jurnal Imiah Perikanan Dan Kelautanah, 13(1), 58–67.
- Ojerio, V. T., Corre Jr, V. L., Toledo, N. A., Andrino-Felarca, K. G. S., Nievales, L. M., & Traifalgar, R. F. M. (2018). Alginic acid as immunostimulant: effects of dose and frequency on growth performance, immune responses, and white spot syndrome virus resistance in tiger shrimp Penaeus monodon (Fabricius, 1798). Aquaculture International, 26(1):267-278.
- Peraza-Gómez, V., Luna-González, A., González-Prieto, J. M., Fierro-Coronado, A., & González-Ocampo, H. A. (2014). Protective effect of microbial immunostimulants and antiviral plants against WSSV in Litopenaeus vannamei cultured under laboratory conditions. Aquaculture, 420-421:160-164.
- Pope, E. C., Powell, A., Roberts, E. C., Shields, E. J., Wardle, R., & Rowley, A. F. (2011). Enhanced cellular immunity in shrimp (Litopenaeus vannamei) after ‘vaccination'. PLoS ONE, 6(6):1-7.
- Rajendran, K. V., Shivam, S., Praveena, P. E., Rajan, J. J. S., Kumar, T. S., Avunje, S., Jagadeesan, V., Babu, S. V. A. N. V. P., Pande, A., Krishnan, A. N., Alavandi, S. V., & Vijayan, K. K. (2016). Emergence of Enterocytozoon hepatopenaei (EHP) in farmed Penaeus (Litopenaeus) vannamei in India. Aquaculture, 454:272-280.
- Sajeevan, T. P., Philip, R., & Bright Singh, I. S. (2009). Dose/frequency: A critical factor in the administration of glucan as immunostimulant to Indian white shrimp Fenneropenaeus indicus. Aquaculture, 287(3-4):248-252.
- Santhoshkumar, S., Sivakumar, S., Vimal, S., Majeed, S. A., Taju, G., Haribabu, P., Uma, A., & Hameed, A. S. S. (2017). Biochemical changes and tissue distribution of Enterocytozoon hepatopenaei (EHP) in naturally and experimentally EHP-infected whiteleg shrimp, Litopenaeus vannamei (Boone, 1931), in India. Journal of Fish Diseases, 40(4):529-539.
- Sung, H. H., Yang, Y. L., & Song, Y. L. (1994). Enhancement of microbicidal activity in the tiger shrimp Penaeus Monodon via immunostimulation. Journal of Crustacean Biology, 16(2):278-284.
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References
Apines-Amar, M. J. S., & Amar, E. C. (2015). Use of immunostimulants in shrimp culture: An update. In C. M. A. Caipang, M. B. I. Bacano-Maningas, & F. F. Fagutao (Ed.), Biotechnological advances in shrimp health management in the Philippines. (pp. 45-71). Kerala, India: Research Signpost.
Aranguren, L. F., Han, J. E., & Tang, K. F. J. (2017). Enterocytozoon hepatopenaei (EHP) is a risk factor for acute hepatopancreatic necrosis disease (AHPND) and septic hepatopancreatic necrosis (SHPN) in the Pacific white shrimp Penaeus vannamei. Aquaculture, 471:37-42.
Babu, D. T., Antony, S. P., Joseph, S. P., Bright, A. R., & Philip, R. (2013). Marine yeast Candida aquaetextoris S527 as a potential immunostimulant in black tiger shrimp Penaeus monodon. Journal of Invertebrate Pathology, 112(3):243-252.
Bairwa, M. K., Jakhar, J. K., Satyanarayana, Y., & Reddy, A. D. (2012). Animal and plant originated immunostimulants used in aquaculture. Journal of Natural Product and Plant Resources, 2(3):397-400.
Barman, D., Nen, P., Mandal, S. C., & Kumar, V. (2013). Immunostimulants for aquaculture health management. Journal of Marine Science: Research & Development, 03(03).
Caro, L. F. A., Mai, H. N., Pichardo, O., Cruz-Flores, R., Hanggono, B., & Dhar, A. K. (2020). Evidences supporting Enterocytozoon hepatopenaei association with white feces syndrome in farmed Penaeus vannamei in Venezuela and Indonesia. Diseases of Aquatic Organisms, 141:71–78.
Citarasu, T., Sivaram, V., Immanuel, G., Rout, N., & Murugan, V. (2006). Influence of selected Indian immunostimulant herbs against white spot syndrome virus (WSSV) infection in black tiger shrimp, Penaeus monodon with reference to haematological, biochemical and immunological changes. Fish and Shellfish Immunology, 21(4):372-384.
Declarador, R. S., Serrano Jr, A. E., & Corre Jr, V. L. (2014). Ulvan extract acts as immunostimulant against white spot syndrome virus (WSSV) in juvenile black tiger shrimp Penaeus monodon. AACL Bioflux, 7(3):153-161.
Desrina, Prayitno, B. B., Haditomo, A. H. C., Latritiani, R., & Sarjito, S. (2020). Detection of Enterocytozoon hepatopenaei (EHP) DNA in the polychaetes from shrimp ponds suffering white feces syndrome outbreaks. Biodiversitas, 21(1):369-374.
Flores-Miranda, M. del C., Luna-González, A., Campa-Córdova, Á. I., González-Ocampo, H. A., Fierro-Coronado, J. A., & Partida-Arangure, B. O. (2011). Microbial immunostimulants reduce mortality in whiteleg shrimp (Litopenaeus vannamei) challenged with Vibrio sinaloensis strains. Aquaculture, 320(1-2):51-55.
Fu, Y. W., Hou, W. Y., Yeh, S. T., Li, C. H., & Chen, J. C. (2007). The immunostimulatory effects of hot-water extract of Gelidium amansii via immersion, injection and dietary administrations on white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish & Shellfish Immunology, 22(6):673-685.
Ganguly, S., Paul, I., & Mukhopadhayay, S. K. (2010). Application and effectiveness of immunostimulants, probiotics, and prebiotics in aquaculture: A review. The Israeli Journal of Aquaculture - Bamidgeh, 62(3):130-138.
Harijanto. (2012). Kemampuan proteksi imunostimulan dari protein membran imunogenik Zoothamnium penaei terhadap Zoothamniosis pada udang vanname (Litopenaeus vannamei). Thesis. Surabaya: Universitas Airlangga.
Hernroth, B., Sköld, H. N., Wiklander, K., Jutfelt, F., & Baden, S. (2012). Simulated climate change causes immune suppression and protein damage in the crustacean Nephrops norvegicus. Fish & Shellfish Immunology, 33(5):1095-1101.
Hidayat, R. P. (2017). Evaluasi pemberian crude protein Zoothamnium penaei Terhadap laju pertumbuhan, respon imun dan kelulushidupan udang vaname (Litopenaeus vannamei) di tambak. Jurnal Biosains Pascasarjana, 19(2):111-132.
Huang, X., Zhou, H., & Zhang, H. (2006). The effect of Sargassum fusiforme polysaccharide extracts on vibriosis resistance and immune activity of the shrimp, Fenneropenaeus chinensis. Fish & Shellfish Immunology, 20(5):750-757.
Jaroenlak, P., Sanguanrut, P., Williams, B. A. P., Stentiford, G. D., Flegel, T. W., Sritunyalucksana, K., & Itsathitphaisarn, O. (2016). A nested PCR assay to avoid false positive detection of the microsporidian Enterocytozoon hepatopenaei (EHP) in environmental samples in shrimp farms. PLoS ONE, 11(11):1-15.
Kumar, S. T., Krishnan, N. A., Rajan, J. S., Makesh, M., Jithendran, K. P., Alavandi, S. V., & Vijayan, K. K. (2018). Visual loop-mediated isothermal amplification (LAMP) for the rapid diagnosis of Enterocytozoon hepatopenaei (EHP) infection. Parasitology Research, 117(5):1485-1493.
Kurcheti, P. P., Mary, A. J., & Dhayanath, M. (2019). Assessment of incidence of Enterocytozoon hepatopenaei (EHP) in Penaeus vannamei in Maharashtra and Gujarat. Journal of Animal Research, 9(4):597-604.
Lowry, Br O. H., Rosebrough, N. J., Farr, A, L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1):265-275.
Maftuch, Prasetio, E., Sudianto, A., Rozik, M., Nurdiyani, R., Sanusi, E., Nursyam, H., Fariedah, F., Marsoedi, & Murachman. (2013). Improvement of innate immune responses and defense activity in tiger shrimp (Penaeus monodon Fab.) by intramuscular administration of the outer membrane protein Vibrio alginolyticus. SpringerPlus, 2(1):1-8.
Mahasri, G., Kusdarwati, R., Kismiyati, Rozi, & Gustrifandi, H. (2018). Effectivity of immunostimulant from Zoothamnium penaei protein membrane for decreasing the mortality rate of white shrimp (Litopenaeus vannamei) in traditional plus pond. IOP Conference Series: Earth and Environmental Science, 137(1).
Mai, H. N., Cruz-Flores, R., Caro, L. F. A., White, B. N., & Dhar, A. K. (2020). A comparative study of Enterocytozoon hepatopenaei (EHP) challenge methods in Penaeus vannamei. Journal of Invertebrate Pathology, 171:107336.
Marimuthu, S., Raju, C. S., & Bhassu, S. (2021). Clinical Investigation and molecular diagnosis of microsporidian Enterocytozoon hepatopenaei (EHP) in shrimps from Selangor, Malaysia. 5(2):67-75.
Marwiyah, U. C., Mahasri, G., Ratnasari, R. E., & Wiradana, P. A. (2019). Total plate count and identification of vibrio in pacific white shrimp (Litophenaeus vannamei) from ponds and in those exposed to immunogenic protein membrane Zoothamnium penaei. IOP Conference Series: Earth and Environmental Science, 236(1):012087.
Mohan, K., Ravichandran, S., Muralisankar, T., Uthayakumar, V., Chandirasekar, R., Seedevi, P., & Rajan, D. K. (2019). Potential uses of fungal polysaccharides as immunostimulants in fish and shrimp aquaculture: A review. Aquaculture, 500:250-263.
Nkuba, A., Gunanti, M., Nunuk, D. R. L., & Adamu Ayubu, M. (2021). Correlation of Nitrite and Ammonia Concentration with Prevalence of. Jurnal Imiah Perikanan Dan Kelautanah, 13(1), 58–67.
Ojerio, V. T., Corre Jr, V. L., Toledo, N. A., Andrino-Felarca, K. G. S., Nievales, L. M., & Traifalgar, R. F. M. (2018). Alginic acid as immunostimulant: effects of dose and frequency on growth performance, immune responses, and white spot syndrome virus resistance in tiger shrimp Penaeus monodon (Fabricius, 1798). Aquaculture International, 26(1):267-278.
Peraza-Gómez, V., Luna-González, A., González-Prieto, J. M., Fierro-Coronado, A., & González-Ocampo, H. A. (2014). Protective effect of microbial immunostimulants and antiviral plants against WSSV in Litopenaeus vannamei cultured under laboratory conditions. Aquaculture, 420-421:160-164.
Pope, E. C., Powell, A., Roberts, E. C., Shields, E. J., Wardle, R., & Rowley, A. F. (2011). Enhanced cellular immunity in shrimp (Litopenaeus vannamei) after ‘vaccination'. PLoS ONE, 6(6):1-7.
Rajendran, K. V., Shivam, S., Praveena, P. E., Rajan, J. J. S., Kumar, T. S., Avunje, S., Jagadeesan, V., Babu, S. V. A. N. V. P., Pande, A., Krishnan, A. N., Alavandi, S. V., & Vijayan, K. K. (2016). Emergence of Enterocytozoon hepatopenaei (EHP) in farmed Penaeus (Litopenaeus) vannamei in India. Aquaculture, 454:272-280.
Sajeevan, T. P., Philip, R., & Bright Singh, I. S. (2009). Dose/frequency: A critical factor in the administration of glucan as immunostimulant to Indian white shrimp Fenneropenaeus indicus. Aquaculture, 287(3-4):248-252.
Santhoshkumar, S., Sivakumar, S., Vimal, S., Majeed, S. A., Taju, G., Haribabu, P., Uma, A., & Hameed, A. S. S. (2017). Biochemical changes and tissue distribution of Enterocytozoon hepatopenaei (EHP) in naturally and experimentally EHP-infected whiteleg shrimp, Litopenaeus vannamei (Boone, 1931), in India. Journal of Fish Diseases, 40(4):529-539.
Sung, H. H., Yang, Y. L., & Song, Y. L. (1994). Enhancement of microbicidal activity in the tiger shrimp Penaeus Monodon via immunostimulation. Journal of Crustacean Biology, 16(2):278-284.
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