Abstract
Carbohydrate metabolism may play an important role in maintaining cell homeostasis in bivalves. In the present study, the temporal variations in immune and carbohydrate metabolism parameters of Zhikong scallop Chlamys farreri under an acute Vibrio anguillarum challenge were investigated in order to better understand the energetic mechanisms of scallop immune defense. After bacterial challenge, reactive oxygen species, total antioxidant capacity, acid phosphatase activity, and transcripts of peptidoglycan recognition protein and heat–shock protein 70 in the hemolymph of scallops increased substantially within 96 h. By contrast, the significantly increased malondialdehyde content was observed in the serum of challenged scallops. As far as carbohydrate metabolism was concerned, the expression levels of hexokinase, isocitrate dehydrogenase, and N-acetylglucosaminyltransferase VI in hemocytes of challenged scallops were significantly up-regulated within 192 h. At 192 h, the electron transport system budgets were significantly higher, while the glycogen contents were significantly lower in soft tissues of challenged scallops as compared to those of control. Moreover, the significantly increased glucose content concomitant with significantly up-regulated expressions of sodium glucose transporter 1 and glucose-regulated protein 78 was observed in the hemolymph at 24 h after challenge. The above results demonstrated that bacterial challenge could induce acute immune responses and cause oxidative stress in scallops. During the bacterial stress period, scallops utilized glucose via anaerobic glycolysis and aerobic oxidation to meet the overall cost of immune response. Also, scallops might rely upon the metabolic pathways of glycogen degradation and gluconeogenesis to maintain glucose homeostasis in hemolymph.
Similar content being viewed by others
References
Ackerman PA, Iwama GK, Thornton JC (2000) Physiological and immunological effects of adjuvanted Aeromonas salmonicida vaccines on juvenile rainbow trout. J Aquat Anim Health 12:157–164
An MI, Choi CY (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comp Biochem Physiol B Biochem Mol Biol 155:34–42
Bachère E, Miahle E, Rodriguez J (1995) Identification of defense effectors in the haemolymph of crustaceans with particular reference to the shrimp Penaeus japonicus (Bate): prospects and application. Fish Shellfish Immunol 5:597–612
Brockhausen I, Hull E, Hindsgaul O, Schachter H, Shah RN, Michnick SW, Carver JP (1989) Control of glycoprotein synthesis. Detection and characterization of a novel branching enzyme from hen oviduct, UDP-N-acetylglucosamine: glcNAcβ1-6 (GlcNAcβ1-2) man α-R (GlcNAc to man) β-4-N-acetylglucosaminyltransferase VI. J Biol Chem 264:11211–11221
Chang M, Wang W, Wang A, Tian T, Wang P, Zheng Y, Liu Y (2009) Effects of cadmium on respiratory burst, intracellular Ca2+ and DNA damage in the white shrimp Litopenaeus vannamei. Comp Biochem Physiol C Toxicol Pharmacol 149:581–586
Cheng P, Liu X, Zhang G, He J (2007) Cloning and expression analysis of a HSP 70 gene from Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol 22:77–87
Cong M, Song L, Wang L, Zhao J, Qiu L, Li L, Zhang H (2008) The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp Biochem Physiol B Biochem Mol Biol 151:191–196
Cramer T, Johnson RS (2003) A novel role for the hypoxia inducible transcription factor HIF-1α. Cell Cycle 2:192–193
Deng H, Cheng Q, Deng LK, Wang SS, Zhou H (2003) Pathogenicity of Vibrio anguillarum and Vibrio nigripulchritudo to larval bay scallop. Fish Sci 22:18–20
Fan Z, Yang A, Lv Z, Liu Z (2007) Effects of Vibrio anguillarum on immune activities of Chlamys farreri. South China Fish Sci 3:52–55
Flye-Sainte-Marie J, Pouvreau S, Paillard C, Jean F (2007) Impact of brown ring disease on the energy budget of the Manila clam Ruditapes philippinarum. J Exp Mar Biol Ecol 349:378–389
Flye-Sainte-Marie J, Jean F, Paillard C, Kooijman SALM (2009) A quantitative estimation of the energetic cost of brown ring disease in the Manila clam using dynamic energy budget theory. J Sea Res 62:114–123
Géret F, Jouan A, Turpin V, Bebianno MJ, Cosson RP (2002) Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquat Living Resour 15:61–66
Haji-Michael PG, Ladriere L, Sener A, Vincent JL, Malaisse WJ (1999) Leukocyte glycolysis and lactate output in animal sepsis and ex vivo human blood. Metabolism 48:779–785
Hall MR, van Ham EH (1998) The effect of different types of stress on blood glucose in the giant tiger prawn Penaeus monodon. J World Aquac Soc 29:290–299
Hanquet A, Jouaux A, Heude C, Mathieu M, Kellner K (2011) A sodium glucose co-transporter (SGLT) for glucose transport into Crassostrea gigas vesicular cells: impact of alimentation on its expression. Aquaculture 313:123–128
Janeway CAJ, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20(1):197–216
Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas JL (2006) Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes Infect 8:2715–2724
Laganà G, Giacobbe S, Bellocco E, Mannucci C, Galtieri A, Ficarra S, Kotyk A, Leuzzi U (2007) Lactate and malate dehydrogenase in the fan-shell associated shrimp, Pontonia pinnophylax (Otto): effects of temperature and urea. J Exp Mar Biol Ecol 349:27–34
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30
Maeng O, Kim YC, Shin HJ, Lee JO, Huh TL, Kang KI, Kim YS, Paik SG, Lee H (2004) Cytosolic NADP+—dependent isocitrate dehydrogenase protects macrophages from LPS-induced nitric oxide and reactive oxygen species. Biochem Biophys Res Commun 317:558–564
Matozzo V, Gallo C, Marin MG (2011) Can starvation influence cellular and biochemical parameters in the crab Carcinus aestuarii? Mar Environ Res 71:207–212
Morel F, Doussiere J, Vignais PV (1991) The superoxide-generating oxidase of phagocytic cells: physiological, molecular and pathological aspects. Eur J Biochem 201:523–546
Patrick S, Faury N, Goulletquer P (2006) Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Oléron bay (France). Aquaculture 252:328–338
Plana S, Sinquin G, Maes P, Paillard C, Pennec ML (1996) Variations in biochemical composition of juvenile Ruditapes philippinarum infected by a Vibrio sp. Dis Aquat Org 24:205–213
Shin SW, Kil IS, Park JW (2010) Cytosolic NADP+-dependent isocitrate dehydrogenase regulates cadmium-induced apoptosis. Biochem Pharmacol 79:1072–1080
Taguchi T, Ogawa T, Inoue S, Inoue Y, Sakamoto Y, Korekane H, Taniguchi N (2000) Purification and characterization of UDP-GlcNAc: glcNAcb1-6(GlcNAcb1-2) Mana1-R [GlcNAc to Man]-b1, 4-N-acetylglucosaminyltransferase VI from hen oviduct. J Biol Chem 275:32598–32602
Thomas JD, Kowalczyk C, Somasundaram B (1990) The biochemical ecology of Biomphalaria glabrata, a freshwater pulmonate mollusc: the uptake and assimilation of exogenous glucose and maltose. Comp Biochem Physiol A Physiol 95:511–528
Tiwari S, Singh A (2005) Alterations in carbohydrates and the protein metabolism of the harmful freshwater vector snail Lymnaea acuminata induced by the Euphorbia tirucalli latex extract. Environ Res 99:378–386
van Rensburg MJ, Coyne VE (2009) The role of electron transport in the defence response of the South African abalone, Haliotis midae. Fish Shellfish Immunol 26:171–176
Wang K (2007) Effects of ammonia on some tissue and haematological parameters of juvenile carp (Cyprinus carpio Linnaeus). Master’s thesis, Northeast Agricultural University
Wang XQ, Wang LL, Yao C, Qiu LM, Zhang H, Zhou Z, Song LS (2012a) Alternation of immune parameters and cellular energy allocation of Chlamys farreri under ammonia-N exposure and Vibrio anguillarum challenge. Fish Shellfish Immunol 32:741–749
Wang X, Wang L, Zhang H, Ji Q, Song L, Qiu L, Zhou Z, Wang M, Wang L (2012b) Immune response and energy metabolism of Chlamys farreri under Vibrio anguillarum challenge and high temperature exposure. Fish Shellfish Immunol 33:1016–1026
Wang L, Qiu L, Zhou Z, Song L (2013) Research progress on the mollusc immunity in China. Dev Comp Immunol 39:2–10
Xiao J, Ford SE, Yang HS, Zhang GF, Zhang FS, Guo XM (2005) Studies on mass summer mortality of cultured zhikong scallops (Chlamys farreri Jones et Preston) in China. Aquaculture 250:602–615
Yang J, Wang W, Wei X, Qiu L, Wang L, Zhang H, Song L (2010) Peptidoglycan recognition protein of Chlamys farreri (CfPGRP-S1) mediates immune defenses against bacterial infection. Dev Comp Immunol 34:1300–1307
Yoganandhan K, Thirupathi S, Sahul Hameed AS (2002) Biochemical, physiological and hematological changes in white spot syndrome virus-infected shrimp, Penaeus indicus. Aquaculture 62:1–11
Zhang W, Wu X, Sun J, Li D (2006) Epizootiological study on mass mortality of the cultured scallop Chlamys farreri. Acta Oceanol Sin 28:90–100
Zhou J, Zhu X, Cai Z (2010) Tributyltin toxicity in abalone (Haliotis diversicolor supertexta) assessed by antioxidant enzyme activity, metabolic response, and histopathology. J Hazard Mater 183:428–433
Zhou Z, Wang L, Shi X, Zhang H, Gao Y, Wang M, Kong P, Qiu L, Song L (2011) The modulation of catecholamines to the immune response against bacteria Vibrio anguillarum challenge in scallop Chlamys farreri. Fish Shellfish Immunol 31:1065–1071
Acknowledgments
The authors are grateful to all the laboratory members for continuous technical advice and helpful discussions. The authors are also grateful to Professor Zhaolan Mo in IOCAS for kindly providing strain of V. anguillarum. This research was supported by 973 National Key Fundamental Research Program (No. 2010CB126404) from the Chinese Ministry of Science and Technology, and a Grant (No. JQ201110) from Shandong Provincial Natural Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, X., Wang, L., Zhang, H. et al. The carbohydrate metabolism of scallop Chlamys farreri in the immune response against acute challenge of Vibrio anguillarum . Aquacult Int 23, 1141–1155 (2015). https://doi.org/10.1007/s10499-014-9871-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-014-9871-6