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HUO Zhongming, MENG Xiangyu, Md. Golam RBBANI, CAO Weinan, WU Qidi, LI Ying, WANG Jingtian, YUAN Hongmei, YANG Feng, YAN Xiwu. Seawater acidification affects the immune enzyme activities of the Manila clam Ruditapes philippinarum[J]. HaiyangYuHuZhao, 2018, 36(5): 1688-1696

Seawater acidification affects the immune enzyme activities of the Manila clam Ruditapes philippinarum

HUO Zhongming, MENG Xiangyu, Md. Golam RBBANI, CAO Weinan, WU Qidi, LI Ying, WANG Jingtian, YUAN Hongmei, YANG Feng, YAN Xiwu
Engineering Research Center of Shellfish Culture and Breeding in Liaoning Province, College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China
Ocean acidification leads to changes in physiological and immune responses of bivalves, but the effect on the immune enzyme activities of the Manila clam, Ruditapes philippinarum, when the pH is lower than the normal value has not been studied in detail. In this study, experiments were conducted to determine how pH (7.4, 7.7, 8.0) affects the immune enzyme activities in the gill and hemocytes of the Manila clam. Membrane stability and phagocytosis increased with decrease of pH from 8.0 to 7.7 and then decreased at pH 7.4. The total protein content in the hemocytes and gills decreased with decreasing pH. Lysozyme content in the hemocytes increased with decreasing pH, and the differences were significant among the different pH groups (P<0.05). Adenosine triphosphatase activity at pH 7.4 was significantly higher than in the other two groups, but no significant difference was observed between pH 7.7 and 8.0. Catalase activity decreased from pH 8.0 to 7.7 and then increased at pH 7.4, and the differences were significant among the experimental groups (P<0.05). These findings provide valuable information about the immune response of R. philippinarum to reduced water pH and insights for future research investigating exposure of bivalves to elevated CO2 conditions.
Key words:    seawater acidification|immune enzyme|Ruditapes philippinarum   
Received: 2017-07-01   Revised:
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Barnhart M C. 1989. Respiratory acidosis and metabolic depression in dormant invertebrates. In:Malan A, Canguilhem B eds. Living in the Cold, Ⅱ. John Libbey Eurotext, London. p.321-331.
Bibby R, Widdicombe S, Parry H, Spicer J, Pipe R. 2008.Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis. Aquatic Biology, 2:67-74.
Caldeira K, Wickett M E. 2003. Oceanography:anthropogenic carbon and ocean pH. Nature, 425(6956):365.
Cheng T C, Rodrick G E. 1975. Lysosomal and other enzymes in the hemolymph of Crassostrea virginica and Mercenaria mercenaria. Comparative Biochemistry and Physiology Part B:Comparative Biochemistry, 52(3):443-447.
Clements J C, Hunt H L. 2017. Effects of CO2-driven sediment acidification on infaunal marine bivalves:a synthesis.Marine Pollution Bulletin, 117(1-2):6-16.
De Souza B K, Jutfelt F, Kling P, Förlin L, Sturve J. 2014.Effects of increased CO2 on fish gill and plasma proteome. PLoS One, 9(7):e102901.
Deigweiher K, Koschnick N, Pörtner H O, Lucassen M. 2008. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 295(5):R1 660-R1 670.
Ding Z K, Li H H, Xu Y Q. 2012. Effect of ocean acidification on respiratory metabolism of marine living things. Feed Industry, 33(20):15-17. (in Chinese with English abstract)
Estrada N, De Jesús Romero M, Campa-Córdova A, Luna A, Ascencio F. 2007. Effects of the toxic dinoflagellate, Gymnodinium catenatum on hydrolytic and antioxidant enzymes, in tissues of the giant lions-paw scallop Nodipecten subnodosus. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 146(4):502-510.
Fan Z J, Yang A G, Liu Z H, Dai J X, Dong Y H, Ren J F. 2006. Effect of pH on the immune factors of Chlamys farreri. Journal of Fishery Sciences of China, 13(4):650-654. (in Chinese with English abstract)
Feely R A, Sabine C L, Lee K, Berelson W, Kleypas J, Fabry V J, Millero F J. 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science, 305(5682):362-366.
Feng S Y. 1988. Cellular defense mechanism of oysters and mussels. Management of Asian Reservoir Fisheries, 18:153-168.
Geracitano L A, Monserrat J M, Bianchini A. 2004. Oxidative stress in Laeonereis acuta (Polychaeta, Nereididae):environmental and seasonal effects. Marine Environmental Research, 58(2-5):625-630.
Hu M H, Lin D H, Shang Y Y, Hu Y, Lu W Q, Huang X Z, Ning K, Chen Y M, Wang Y J. 2017. CO2-induced pH reduction increases physiological toxicity of nano-TiO2 in the mussel Mytilus coruscus. Scientific Reports, 7:40 015,
Huang X Z, Lin D H, Ning K, Sui Y M, Hu M H, Lu W Q, Wang Y J. 2016. Hemocyte responses of the thick shell mussel Mytilus coruscus exposed to nano-TiO2 and seawater acidification. Aquatic Toxicology, 180:1-10.
Inoue S, Oshima Y, Usuki H, Hamaguchi M, Hanamura Y, Kai N, Shimasaki Y, Honjo T. 2007. Effect of tributyltin on veliger larvae of the Manila clam, Ruditapes philippinarum. Chemosphere, 66(7):1 353-1 357.
Ishimatsu A, Hayashi M, Lee K S, Kikkawa T, Kita J. 2005. Physiological effects on fishes in a high-CO2 world. Journal of Geophysical Research:Oceans, 110(C9):C09S09.
Lannig G, Eilers S, Pörtner H O, Sokolova I M, Bock C. 2010. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas-changes in metabolic pathways and thermal response. Marine Drugs, 8(8):2 318-2 339.
Li J Q, Jiang Z J, Zhang J H, Mao Y Z, Bian D P, Fang J G. 2014. The potential of ocean acidification on suppressing larval development in the Pacific oyster Crassostrea gigas and blood cockle Arca inflata Reeve. Chinese Journal of Oceanology and Limnology, 32(6):1 307-1 313.
Lin S Q, Lan R F, Yu P, Cheng W. 2000. Purification and partial characteristics of the catalase from Perna viridis. Food Science, 21(11):22-24.
Liu Z H, Mou H J, Wang Q Y. 2003. Research progress of immune related enzymes in mollusca. Marine Fisheries Research, 24(3):86-90. (in Chinese with English abstract)
Marchant H K, Calosi P, Spicer J I. 2010. Short-term exposure to hypercapnia does not compromise feeding, acid-base balance or respiration of Patella vulgata but surprisingly is accompanied by radula damage. Journal of the Marine Biological Association of the United Kingdom, 90(7):1 379-1 384.
Matozzo V, Chinellato A, Munari M, Finos L, Bressan M, Marin M G. 2012. First evidence of immunomodulation in bivalves under seawater acidification and increased temperature. PLoS One, 7(3):e33820.
Melzner F, Göbel S, Langenbuch M, Gutowska M A, Pörtner H O, Lucassen M. 2009. Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4-12 months) acclimation to elevated seawater Pco2. Aquatic Toxicology, 92(1):30-37.
Meseck S L, Alix J H, Swiney K M, Long W C, Wikfors G H, Foy R J. 2016. Ocean acidification affects hemocyte physiology in the tanner crab (Chionoecetes bairdi). PLoS One, 11(2):e0148477.
Michaelidis B, Ouzounis C, Paleras A, Pörtner H O. 2005. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series, 293:109-118.
Paillard C. 2004. A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus. Aquatic Living Resources, 17(4):467-475.
Parker L M, Ross P M, O'Connor W A, Pöertner H O, Scanes E, Wright J M. 2013. Predicting the response of molluscs to the impact of ocean acidification. Biology, 2(2):651-692.
Parvez S, Sayeed I, Raisuddin S. 2006. Decreased gill ATPase activities in the freshwater fish Channa punctata (Bloch) exposed to a diluted paper mill effluent. Ecotoxicology and Environmental Safety, 65(1):62-66.
Pörtner H O, Finke E, Lee P G. 1996. Metabolic and energy correlates of intracellular pH in progressive fatigue of squid (L. brevis) mantle muscle. The American Journal of Physiology, 271(5):R1 403-R1 414.
Pörtner H O, Langenbuch M, Reipschläger A. 2004. Biological impact of elevated ocean CO2 concentrations:lessons from Animal Physiology and Earth History. Journal of Oceanography, 60(4):705-718.
Qiu J B, Ma F F, Fan H, Li A F. 2013. Effects of feeding Alexandrium tamarense, a paralytic shellfish toxin producer, on antioxidant enzymes in scallops(Patinopecten yessoensis) and mussels (Mytilus galloprovincialis). Aquaculture, 396-399:76-81.
Rees B B, Hand S C. 1990. Heat dissipation, gas exchange and acid-base status in the land snail Oreohelix during shortterm estivation. Journal of Experimental Biology, 152:77-92.
Sabine C L, Feely R A, Gruber N, Key R M, Lee K, Bullister J L, Wanninkhof R, Wong C S, Wallace D W R, Tilbrook B, Millero F J, Peng T H, Kozyr A, Ono T, Rios A F. 2004. The oceanic sink for anthropogenic CO2. Science, 305(5682):367-371.
Saxena T B, Zachariassen K E, Jørgensen L. 2000. Effects of ethoxyquin on the blood composition of turbot, Scophthalmus maximus L. Comparative Biochemistry and Physiology Part C:Pharmacology, Toxicology and Endocrinology, 127(1):1-9.
Seidelin M, Brauner C J, Jensen F B, Madsen S S. 2001. Vacuolar-type H+-ATPase and Na+, K+-ATPase expression in gills of Atlantic salmon (Salmo salar) during isolated and combined exposure to hyperoxia and hypercapnia in fresh water. Zoological Science, 18(9):1 199-1 205.
Sui Y M, Hu M H, Shang Y Y, Wu F L, Huang X Z, Dupont S, Storch D, Pörtner H O, Li J L, Lu W Q, Wang Y J. 2017. Antioxidant response of the hard shelled mussel Mytilus coruscus exposed to reduced pH and oxygen concentration. Ecotoxicology and Environmental Safety, 137:94-102.
Sui Y M, Kong H, Huang X Z, Dupont S, Hu M H, Storch D, Pörtner H O, Lu W Q, Wang Y J. 2016b. Combined effects of short-term exposure to elevated CO2 and decreased O2 on the physiology and energy budget of the thick shell mussel Mytilus coruscus. Chemosphere, 155:207-216.
Sui Y M, Kong H, Shang Y Y, Huang X Z, Wu F L, Hu M H, Lin D H, Lu W Q, Wang Y J. 2016a. Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Marine Pollution Bulletin, 108(1-2):46-52.
Sun T L, Tang X X, Jiang Y S, Wang Y. 2017. Seawater acidification induced immune function changes of haemocytes in Mytilus edulis:a comparative study of CO2 and HCl enrichment. Scientific Reports, 7:41 488.
Sun Y Y, Gao R C, Wen Y M, Chen N, Wang S. 2008. Effects of temperature on hydrolase and antioxidase activities in liver of clam Hiatula chinensis and H. diphos. Fisheries Science, 27(10):543-544. (in Chinese with English abstract)
Talmage S C. 2011. The Effects of Elevated Carbon Dioxide Concentrations on the Early Life History of Bivalve Shellfish. The Graduate School, Stony Brook University:Stony Brook, NY.
Taucher J, Haunost M, Boxhammer T, Bach L T, Algueró-Muñiz M, Riebesell U. 2017. Influence of ocean acidification on plankton community structure during a winter-to-summer succession:an imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects. PLoS One, 12(2):e0169737.
Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A. 2007. The use of biomarkers in biomonitoring:a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 146(3):281-300.
Wang Y J, Li L S, Hu M H, Lu W Q. 2015. Physiological energetics of the thick shell mussel Mytilus coruscus exposed to seawater acidification and thermal stress. Science of the Total Environment, 514:261-272.
Winston G W, Moore M N, Kirchin M A, Soverchia C. 1996. Production of reactive oxygen species by Hemocytes from the marine mussel, Mytilus edulis:lysosomal localization and effect of xenobiotics. Comparative Biochemistry and Physiology Part C:Pharmacology, Toxicology and Endocrinology, 113(2):221-229.
Wu F L, Lu W Q, Shang Y Y, Kong H, Li L S, Sui Y M, Hu M H, Wang Y J. 2016. Combined effects of seawater acidification and high temperature on hemocyte parameters in the thick shell mussel Mytilus coruscus.Fish & Shellfish Immunology, 56:554-562.
Xiao X, Deng R P, Chen Z L, Han Y L. 2003. Characteristics study on Oyster catalase and Tegillarca granosa catalase. Food Science, 24(9):32-34. (in Chinese with English abstract)
Xu X, Yang F, Zhao L Q, Yan X W. 2016. Seawater acidification affects the physiological energetics and spawning capacity of the Manila clam Ruditapes philippinarum during gonadal maturation. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 196:20-29.
Yadwad V B, Kallapur V L, Basalingappa S. 1990. Inhibition of gill Na+K+-ATPase activity in dragonfly larva, Pantala flavesens, by endosulfan. Bulletin of Environmental Contamination and Toxicology, 44(4):585-589.
Yan X W, Zhang Y H, Huo Z M, Yang F, Zhang G F. 2009.Effects of starvation on larval growth, survival, and metamorphosis of Manila clam Ruditapes philippinarum.Acta Ecologica Sinica, 29(6):327-334.
Zhao X G, Chai X L, Xiao G Q, Sun C S, Liu G X. 2012.Effects of ocean acidification on intertidal shellfish fertilization research. In:Proceedings of 2012 Abstracts of the 2012 Annual Meeting of China Environmental Science Society Marine Environmental Protection Specialized Committee. Chinese Society for Oceanology and Limnology, Chinese Society for Environmental Sciences, Yanji. (in Chinese)