Eff ect of Diurnal Temperature Change on Growth and Pir Toxin Production of Vibrio parahaemolyticus Causing Acute Hepatopancreatic Necrosis Disease (AHPND)
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Published:
Dec 28, 2018
Keywords:
Acute Hepatopancreatic Necrosis Disease (AHPND); Vibrio parahaemolyticus; Diurnal Temperature Change, Photorhabdus Insect-related (Pir) Toxin, Specifi c Growth Rate
Main Article Content
Abstract
The culture of white shrimp (Litopenaeus vannamei) in Thailand has encountered an acute hepatopancreatic necrosis disease (AHPND) since 2013 resulting in a devastating reduction of white shrimp production. The infection of Vibrio parahaemolyticus of which strains carrying plasmids with the genes encoding the Photorhabdus insect-related (Pir) A toxin and Pir B toxin are considered as a cause of this epidemic disease. Recently, a number of environmental factors have been reported to influence the spread of disease. This research work aimed to study the variation patterns of water temperature in white shrimp culturing pond throughout the day and night. The effect of the diurnal temperature change on the growth of AHPND-causing V. parahaemolyticus was also determined. After collecting the data of water temperature in white shrimp culturing ponds in 2017, we classified the temperature variation patterns into 3 major groups; (1) normal temperature range (24 - 30 oC), (2) low temperature range (22 - 27 oC) and (3) fluctuating temperature range (22 - 30 oC). These 3 diurnal temperature patterns were set to continually culture V. parahaemolyticus strain causing AHPND for 24 h and the comparative analysis of bacterial growth and specific
growth rate was performed. The results showed that the bacterial growths were similar while the specific growth rates were different. The fluctuating temperature range especially that of the variation range of 3 oC caused the greatest specific growth rate. Moreover, the produced proteins including Pir A and Pir B toxins in the bacterial culture media in 3 temperature patterns were also determined via SDS-PAGE. The obtained results suggested that the temperature change could affect the growth and toxin production as well as involve in pathogenicity of AHPND-causing V. parahaemolyticus. This knowledge leads to the cultural and farm management practices to efficient reduce losses caused by the AHPND.
Article Details
How to Cite
[1]
จิรพงศธรกุล น., รัตนาภรณ์ อ., แพรกทอง พ., and อุเทนะพันธุ์ ก., “Eff ect of Diurnal Temperature Change on Growth and Pir Toxin Production of Vibrio parahaemolyticus Causing Acute Hepatopancreatic Necrosis Disease (AHPND)”, RMUTI Journal, vol. 11, no. 3, pp. 70–88, Dec. 2018.
Section
Research article
References
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[14] Lafferty, K. D. (2009). The Ecology of Climate Change and Infectious Diseases. Ecology. Vol. 90, Issue 4, pp. 888-900. DOI: 10.1890/08-0079.1
[15] Guerreiro, I., Pérez-Jiménez, A., Costas, B., and Oliva-Teles, A. (2014). Effect of Temperature and Short Chain Fructooligosaccharides Supplementation on the Hepatic Oxidative Status and Immune Response of Turbot (Scophthalmus maximus). Fish & Shellfish Immunology. Vol. 40, Issue 2, pp. 570-576. DOI: 10.1016/j.fsi.2014.08.017
[16] Yu, H. B., Kaur, R., Lim, S. M., Wang, X. H., and Leung, K. Y. (2007). Characterization of Extracellular Proteins Produced by Aeromonas hydrophila AH-1. Proteomics. Vol. 7, No. 3, pp. 436-449. DOI: 10.1002/pmic.200600396
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[18] Chase, E. and Harwood, V. J. (2011). Comparison of the Effects of Environmental Parameters on Growth Rates of Vibrio vulnificus Biotypes I, II, and III by Culture and Quantitative PCR Analysis. Applied and Environmental Microbiology. Vol. 77, No. 12, pp. 4200-4207. DOI: 10.1128/AEM.00135-11
[19] Kim, Y. W., Lee, S. H., Hwang, I. G., and Yoon, K. S. (2012). Effect of Temperature on Growth of Vibrio paraphemolyticus and Vibrio vulnificus in Flounder, Salmon Sashimi and Oyster Meat. International Journal of Environmental Research and Public Health. Vol. 9, No. 12, pp. 4662-4675. DOI: 10.3390/ijerph9124662
[20] Mudoh, M. F., Parveen, S., Schwarz, J., Rippen, T., and Chaudhuri, A. (2014). The Effects of Storage Temperature on the Growth of Vibrio parahaemolyticus and Organoleptic Properties in Oysters. Frontiers in Public Health. Vol. 2, DOI: 10.3389/fpubh.2014.00045
[21] Tarr, C. L., Patel, J. S., Puhr, N. D., Sowers, E. G., Bopp, C. A., and Strockbine, N. A. (2007). Identifi cation of Vibrio Isolates by a Multiplex PCR Assay and rpoB Sequence Determination. Journal of Clinical Microbiology. Vol. 45, No. 1, pp. 134-140. DOI: 10.1128/JCM.01544-06
[22] Bradford, M. M. (1979). A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Proteins Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry. Vol. 72, Issue 1-2, pp. 248-254
[23] Laemmli, U. K. (1970). Cleavage of Structural Proteins during Assembly of Head of Bacteriophage T4. Nature. Vol. 227, pp. 680-685
[24] Lee, C. -T., Chen, I. -T., Yang, Y. -T., Ko, T. -P., Huang, Y. -T., Huang, J. -Y., Huang, M. -F., Lin, S. -J., Chen, C. -Y., Lin, S. -S., Lightner, D. V., Wang, H. -C., Wang, A. H., Wang, H. -C., Hor, L. -I., and Lo, C. -F. (2015). The Opportunistic Marine Pathogen Vibrio parahaemolyticus Becomes Virulent by Acquiring a Plasmid that Expresses a Deadly Toxin. In Proceedings of the National Academy of Sciences of the United States of America. Vol. 112, No. 34, pp. 10798-10803. DOI: 10.1073/pnas.1503129112
[25] Maier, R. M. (2000). Bacterial Growth. In Environmental Microbiology. Maier, R.M., Pepper, I.L. and Gebra C.P., eds. pp. 43-59. Academic Press
[26] Zwietering, I., De Wit, J. C., Cuppers, H. G. A. M., and Van ‘T Riet, K. (1994). Modeling of Bacterial Growth with Shifts in Temperature. Applied and Environmental Microbiology. Vol. 60, No. 1, pp. 204-213
[27] Van Derlinden, E., Bernaerts, K, and Van Impe, J. F. (2008). Dynamics of Escherichia coli at Elevated Temperatures: Effect of Temperature History and Medium. Journal of Applied Microbiology. Vol. 104, No. 2, pp. 438-453. DOI: 10.1111/j.1365-2672.2007.03592.x
[28] Zotta, T., Guidone, A., Ianniello, R. G., Parente, E., and Ricciardi, A. (2013). Temperature and Respiration Affect the Growth and Stress Resistance of Lactobacillus plantarum C17. Journal of Applied Microbiology. Vol. 115, No. 3, pp. 848-858. DOI: 10.1111/jam.12285
[29] Soberón, M., Pardo, L., Muñóz-Garay, C., Sánchez, J., Gómez, I., Porta, H., and Bravo, A. (2010). Pore Formation by Cry Toxins. Advances in Experimental Medicine and Biology. Vol. 677, pp. 127-142
[2] Fisheries Statistics Analysis and Research Group, Fisheries Development Policy and Strategy Division. (2017). Statistics of Marine Shrimp Culture 2015. Department of Fisheries Ministry of Agriculture and Cooperatives. No. 2, pp. 1-46 (in Thai)
[3] Tran, L., Nunan, L., Redman, R. M., Mohney, L. L., Pantoja, C. R., Fitzsimmons, K., and Lightner, D. V. (2013). Determination of the Infectious Nature of the Agent of Acute Hepatopancreatic Necrosis Syndrome Affecting Penaeid Shrimp. Diseases of Aquatic Organisms. Vol. 105, Issue 1, pp. 45-55
[4] Joshi, J., Srisala, J., Truong, V. H., Chen, I. T., Nuangsaeng, B., Suthienkul, O., Lo, C. F., Flegel, T. W., Sritunyalucksana, K., and Thitamadee, S. (2014). Variation in Vibrio parahaemolyticus Isolates from a Single Thai Shrimp Farm Experiencing an Outbreak of Acute Hepatopancreatic Necrosis Disease (AHPND). Aquaculture. Vol. 428-429, pp. 297-302. DOI: 10.1016/j.aquaculture.2014.03.030
[5] Dangtip, S., Sirikharin, R., Sanguanrut, P., Thitamadee, S., Sritunyalucksana, K., Taengchaiyaphum, S., Mavichak, R., Proespraiwong, P., and Flegel, T. W. (2015). AP4 Method for Two-Tube Nested PCR Detection of AHPND Isolates of Vibrio parahaemolyticus. Aquaculture Reports. Vol. 2, pp. 158-162. DOI: 10.1016/j.aqrep.2015.10.002
[6] Sirikharin, R., Taengchaiyaphum, S., Sanguanrut, P., Chi, T. D., Mavichak, R., Proespraiwong, P., Nuangsaeng, B., Thitamadee, S., Flegel, T. W., and 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. Vol. 10(5). DOI:10.1371/journal.pone. 0126987
[7] Xiao, J., Liu, L., Ke, Y., Li, X., Liu, Y., Pan, Y., Yan, S., and Wang, Y. (2017). Shrimp AHPND-Causing Plasmids Encoding the PirAB Toxins as Mediated by PirAB-Tn903 are Prevalent in Various Vibrio species. Scientific Reports. Vol. 7, Article number: 42177. DOI: 10.1038/srep42177
[8] Boonyawiwat, V., Patanasatienkul, T., Kasornchandra, J., Poolkhet, C., Yaemkasem, S., Hammell, L., and Davidson, J. (2017). Impact of Farm Management on Expression of Early Mortality Syndrome/Acute Hepatopancreatic Necrosis Disease (EMS/AHPND) on Penaeid Shrimp Farms in Thailand. Journal of Fish Diseases. Vol. 40, Issue 5, pp. 649-659. DOI: 10.1111/jfd.12545
[9] Chumpol, S., Kantachote, D., Nitoda, T. and Kanzaki, H. (2017). The Roles of Probiotic Purple Nonsulfur Bacteria to Control Water Quality and Prevent Acute Hepatopancreatic Necrosis Disease (AHPND) for Enhancement Growth with Higher Survival in White Shrimp (Litopenaeus vannamei) during Cultivation. Aquaculture. Vol. 473, pp. 327-336. DOI: 10.1016/j.aquaculture.2017.02.033
[10] Chen, W. -Y., Ng, T. H., Wu, J. -H., Chen, J. -W., and Wang, H. -C. (2017). Microbiome Dynamics in a Shrimp Grow-Out Pond with Possible Outbreak of Acute Hepatopancreatic Necrosis Disease. Scientific Reports. Vol. 7, No. 1, Article number: 9395. DOI: 10.1038/s41598-017-09923-6
[11] Tinwongger, S., Proespraiwong, P., Thawonsuwan, J., Sriwanayos, P., Kongkumnerd, J., Chaweepack, T., Mavichak, R., Unajak, S., Nozaki, R., Kondo, H., and Hirono, I. (2014). Development of PCR Diagnosis for Shrimp Acute Hepatopancreatic Necrosis Disease (AHPND) Strain of Vibrio parahaemolyticus. Fish Pathology. Vol. 49, Issue 4, pp. 159-164. DOI: 10.3147/jsfp.49.159
[12] Thakur, D. P. and Lin, C. K. (2003). Water Quality and Nutrient Budget in Close Shrimp (Penaeus monodon) Culture Systems. Aquaculture Research. Vol. 27, No. 3, pp. 159-176
[13] Akazawa, N. and Eguchi, M. (2017). Pond Sludge and Increased pH Cause Early Mortality Syndrome/Acute Hepatopancreatic Necrosis Disease (EMS/AHPND) in Cultured White Shrimp. Borneo Journal of Marine Science and Aquaculture. Vol. 1, pp. 92-96
[14] Lafferty, K. D. (2009). The Ecology of Climate Change and Infectious Diseases. Ecology. Vol. 90, Issue 4, pp. 888-900. DOI: 10.1890/08-0079.1
[15] Guerreiro, I., Pérez-Jiménez, A., Costas, B., and Oliva-Teles, A. (2014). Effect of Temperature and Short Chain Fructooligosaccharides Supplementation on the Hepatic Oxidative Status and Immune Response of Turbot (Scophthalmus maximus). Fish & Shellfish Immunology. Vol. 40, Issue 2, pp. 570-576. DOI: 10.1016/j.fsi.2014.08.017
[16] Yu, H. B., Kaur, R., Lim, S. M., Wang, X. H., and Leung, K. Y. (2007). Characterization of Extracellular Proteins Produced by Aeromonas hydrophila AH-1. Proteomics. Vol. 7, No. 3, pp. 436-449. DOI: 10.1002/pmic.200600396
[17] Yoon, K. S., Min, K. J., Jung, Y. J., Kwon, K. Y., Lee, J. K., and Oh, S. W. (2008). A Model of the Effect of Temperature on the Growth of Pathogenic and Nonpathogenic Vibrio parahaemolyticus Isolated from Oysters in Korea. Food Microbiology. Vol. 25, Issue 5, pp. 635-641. DOI: 10.1016/j.fm.2008.04.007
[18] Chase, E. and Harwood, V. J. (2011). Comparison of the Effects of Environmental Parameters on Growth Rates of Vibrio vulnificus Biotypes I, II, and III by Culture and Quantitative PCR Analysis. Applied and Environmental Microbiology. Vol. 77, No. 12, pp. 4200-4207. DOI: 10.1128/AEM.00135-11
[19] Kim, Y. W., Lee, S. H., Hwang, I. G., and Yoon, K. S. (2012). Effect of Temperature on Growth of Vibrio paraphemolyticus and Vibrio vulnificus in Flounder, Salmon Sashimi and Oyster Meat. International Journal of Environmental Research and Public Health. Vol. 9, No. 12, pp. 4662-4675. DOI: 10.3390/ijerph9124662
[20] Mudoh, M. F., Parveen, S., Schwarz, J., Rippen, T., and Chaudhuri, A. (2014). The Effects of Storage Temperature on the Growth of Vibrio parahaemolyticus and Organoleptic Properties in Oysters. Frontiers in Public Health. Vol. 2, DOI: 10.3389/fpubh.2014.00045
[21] Tarr, C. L., Patel, J. S., Puhr, N. D., Sowers, E. G., Bopp, C. A., and Strockbine, N. A. (2007). Identifi cation of Vibrio Isolates by a Multiplex PCR Assay and rpoB Sequence Determination. Journal of Clinical Microbiology. Vol. 45, No. 1, pp. 134-140. DOI: 10.1128/JCM.01544-06
[22] Bradford, M. M. (1979). A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Proteins Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry. Vol. 72, Issue 1-2, pp. 248-254
[23] Laemmli, U. K. (1970). Cleavage of Structural Proteins during Assembly of Head of Bacteriophage T4. Nature. Vol. 227, pp. 680-685
[24] Lee, C. -T., Chen, I. -T., Yang, Y. -T., Ko, T. -P., Huang, Y. -T., Huang, J. -Y., Huang, M. -F., Lin, S. -J., Chen, C. -Y., Lin, S. -S., Lightner, D. V., Wang, H. -C., Wang, A. H., Wang, H. -C., Hor, L. -I., and Lo, C. -F. (2015). The Opportunistic Marine Pathogen Vibrio parahaemolyticus Becomes Virulent by Acquiring a Plasmid that Expresses a Deadly Toxin. In Proceedings of the National Academy of Sciences of the United States of America. Vol. 112, No. 34, pp. 10798-10803. DOI: 10.1073/pnas.1503129112
[25] Maier, R. M. (2000). Bacterial Growth. In Environmental Microbiology. Maier, R.M., Pepper, I.L. and Gebra C.P., eds. pp. 43-59. Academic Press
[26] Zwietering, I., De Wit, J. C., Cuppers, H. G. A. M., and Van ‘T Riet, K. (1994). Modeling of Bacterial Growth with Shifts in Temperature. Applied and Environmental Microbiology. Vol. 60, No. 1, pp. 204-213
[27] Van Derlinden, E., Bernaerts, K, and Van Impe, J. F. (2008). Dynamics of Escherichia coli at Elevated Temperatures: Effect of Temperature History and Medium. Journal of Applied Microbiology. Vol. 104, No. 2, pp. 438-453. DOI: 10.1111/j.1365-2672.2007.03592.x
[28] Zotta, T., Guidone, A., Ianniello, R. G., Parente, E., and Ricciardi, A. (2013). Temperature and Respiration Affect the Growth and Stress Resistance of Lactobacillus plantarum C17. Journal of Applied Microbiology. Vol. 115, No. 3, pp. 848-858. DOI: 10.1111/jam.12285
[29] Soberón, M., Pardo, L., Muñóz-Garay, C., Sánchez, J., Gómez, I., Porta, H., and Bravo, A. (2010). Pore Formation by Cry Toxins. Advances in Experimental Medicine and Biology. Vol. 677, pp. 127-142