Abstract
In this study, changes of reactive oxygen species (ROS) and the mRNA expression of catalase of the Pacific white shrimp, Litopenaeus vannamei, exposed to pH (5.4, 6.7, 8.0, and 9.3) stress was investigated at different stress time (24, 48, 72, 96, and 120 h). Level of malondialdehyde (MDA) in shrimp also were assessed. The results revealed that acidic (pH 5.4 and 6.7) or alkaline exposure (pH 9.3) induced production of ROS hemocytes and increase of MDA level in shrimp. Moreover, the catalase mRNA expression in hepatopancreas of L. vannamei was up-regulated in 24 h at pH 5.4, in 72 h at pH 6.7 and in 48 h at pH 9.3, whereas was down-regulated significantly after 72 h acidic (pH 5.4 and 6.7) or alkaline (pH 9.4) exposure. In the present study, there was the relationship between ROS and catalase mRNA expression under normal acidic and alkaline conditions. At pH 8, the increase of catalase transcripts due to up-regulation by ROS, whereas MDA level did not significantly change, suggesting activation of corresponding protective mechanisms of detoxifying ROS is essential for the proper functioning of cells and the survival of shrimps.
Similar content being viewed by others
References
Anderson RS, Oliver LM, Brubacher LL (1992) Superoxide anion generation by Crassostrea virginica hemocytes as measured by nitrotetrazolium reduction. J Invertebr Pathol 59:303–307
Arun S, Subramanian P (1998) Antioxidant enzymes in freshwater prawn Macrobrachium malcolmsonii during embryonic and larval development. Comp Biochem Physiol B 121:273–277
Arun S, Krishnamoorthy P, Subramanian P (1999) Properties of glutathione peroxidase from hepatopancreas of fresh water prawn Macrobrachium malcolmsonii. Int J Biochem Cell Biol 31:725–732
Bachère E (2000) Shrimp immunity and disease control. Aquaculture 191:3–11
Campa-Córdova AI, Hernández-Saaverdra NY, De Philippis R, Ascencio F (2002) Generation of superoxide anion and SOD activity in haemocytes and muscle of American white shrimp (Litopenaeus vannameii) as a response to b-glucan and sulphated polysaccharide. Fish Shellfish Immunol 12:353–366
Chen JC, Lee Y (1997) Effects of nitrite on mortality, ion regulation and acid-base balance of Macrobrachium rosenbergii at different external chloride concentrations. Aquat Toxicol 39:291–305
Cheng W, Wang CH (2001) The susceptibility of the giant freshwater prawn Macrobrachium rosenbergii to Lactococcus garvieae and its resistance under copper sulfate stress. Dis Aquat Organ 47:137–144
Cheng W, Tung YS, Liu CH, Chen JC (2006) Molecular cloning and characterisation of cytosolic manganese superoxide dismutase (cytMn-SOD) from the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol 20:438–449
Fang YZ, Yang S, Wu GY (2002) Free radical, antioxidants and nutrition. Nutrition 18:872–879
Gidron Y, Russ K, Tissarchondon H, Warner J (2006) The relation between psychological factors and DNA-damage: a critical review. Biol Psychol 72:291–304
Gilmour KM, Perry SF (1994) The effects of hypoxia, hyperoxia or hypercapnia on the acid–base disequilibrium in the arterial blood of rainbow trout. J Exp Biol 192:269–284
Gómez-Anduro GA, Barillas-Mury CV, Peregrino-Uriarte AB, Gupta L, Gollas-Galván T, Hernández-López J, Yepiz-Plascencia G (2006) The cytosolic manganese superoxide dismutase from the shrimp Litopenaeus vannameii: molecular cloning and expression. Dev Comp Immunol 30:893–900
González-Flecha B, Demple B (2000) Genetic responses to free radicals. In: Chiueh CC (ed) Reactive oxygen species from radiation to molecular biology. The New York Academy of Sciences, New York
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Clarendon Press, Oxford
Hand S (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233–1242
Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. In: Storey KB (ed) Functional metabolism: regulation and adaptation. Wiley–Liss, Hoboken, pp 319–368
Holmblad T, Söderhäll K (1999) Cell adhesion molecules and antioxidative enzymes in a crustacean, possible role in immunity. Aquaculture 172:111–123
Kumar S, Sahu NP, Pal AK, Choudhury D, Yengkokpam S, Mukherjee SC (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immunol 19:331–344
Kumazawa NH, Morimoto N, Okamoto Y (1993) Luminol-dependent chemiluminescence of hemocytes derived from marine and estuarine molluscs. J Vet Med Sci 55:287–290
Larade K, Storey K (2002) Reversible suppression of protein synthesis in concert with polysome disaggregation during anoxia exposure in Littorina littorea. Mol Cell Biochem 232:121–127
Lee PJ, Choi AMK (2003) Pathways of cell signaling in hyperoxia. Free Radic Biol Med 35:341–350
Lee SY, Söderhäll K (2002) Early events in crustacean innate immunity. Fish Shelfish Immunol 12:421–437
Liu CH, Tseng MC, Cheng W (2007) Identification and cloning of the antioxidant enzyme, glutathione peroxidase, of white shrimp, Litopenaeus vannamei, and its expression following Vibrio alginolyticus infection. Fish Shelfish Immunol 23:34–45
Mohankumar K, Ramasamy P (2006) White spot syndrome virus infection decreases the activity of antioxidant enzymes in Fenneropenaeus indicus. Virus Res 15:69–75
Morgan DO, McMahon BR (1982) Acid tolerance and effects of sulethal acid exposure on iono-regulation and acid–base status in two crayfish Procambarus clarki and Orconectes rusticus. J Exp Biol 97:241–252
Muňoz M, Cedeňo R, Rodríguez J, Van der Knaap WPW, Mialhe E, Bachère E (2000) Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture 191:89–107
Petriv OI, Rachubinski RA (2004) Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J Biol Chem 279:19996–20001
Pipe RK (1992) Generation of reactive oxygen metabolites by the haemocytes of the mussel Mytilus edulis. Dev Comp Immunol 16:111–122
Pipe R, Porte C, Livingstone D (1993) Antioxidant enzymes associated with the blood cells and haemolymph of the mussel Mytilus edulis. Fish Shellfish Immunol 3:221–233
Raquel CS (2006) Mecanismos de adaptación de Saccharomyces cerevisiae a la alcalinización ambiental. TDX-1219106-163252 http://www.tesisenxarxa.net/
Robertson R, El-Haj A, Clarke A, Taylor E (2001) Effects of temperature on specific dynamic action and protein synthesis rates in the Baltic isopod crustacean, Saduria entomon. J Exp Mar Biol Ecol 262:113–129
Roch P (1999) Defense mechanisms and disease prevention in farmed invertebrates. Aquaculture 172:125–145
Röhrdanz E, Obertrifter B, Ohler S, Kahl R (2000) Influence of adriamycin and paraquat on antioxidant enzyme expression in primary rat hepatocytes. Arch Toxicol 74:231–237
Schwarz KB (1996) Oxidative stress during viral infection: a review. Free Radic Biol Med 21:641–649
Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans; does it really protect against infection? Fish Shellfish Immunol 15:71–90
Söderhäll K, Cerenius L (1998) Role of prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28
Storz G, Tartaglia LA, Ames BN (1990) Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248:189–194
Tavares-Sanchez OL, Gomez-Anduro GA, Felipe-Ortega X, Islas-Osuna MA, Sotelo-Mundo RR, Barillas-Mury C, Yepiz-Plascencia G (2004) Catalase from the white shrimp Penaeus (Litopenaeus) vannamei: molecular cloning and protein detection. Comp Biochem Physiol 138:331–337
Uchiyama M, Mihara M (1978) Determination of malondialdehyde precursor in tissues by thiobarbituric acid test. Ann Biochem 86:271–278
Wang WN, Wang AL, Chen L, Liu Y, Sun RY (2002) Effects of pH on survival, phosphorus concentration, adenylate energy charge and Na+–K+ ATPase activities of Penaeus chinensis Osbeck juveniles. Aquat Toxicol 60:75–83
Wang WN, Wang AL, Zhang YJ, Li ZH, Wang JX, Sun RY (2004) Effects of nitrite on lethal and immune response of Macrobrachium nipponense. Aquaculture 232:679–686
Wang WN, Wang AL, Wang Y, Wang JX, Sun RY (2005) Effect of dietary vitamin C and ammonia concentration on the cellular defense response of Macrobrachium nipponense. J World Aquac Soc 36:1–7
Wang WN, Wang AL, Liu Y, Xu J, Sun RY (2006) Effects of temperature on growth, adenosine phosphates, ATPase and cellular defense response of juvenile shrimp Macrobrachium nipponense. Aquaculture 256:624–630
Wang YC, Chang PS, Chen HY (2007) Tissue expressions of nine genes important to immune defence of the Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 23:1161–1177
Wang WN, Zhou J, Wang P, Tian TT, Zheng Y, Liu Y, Mai WJ, Wang AL (2009) Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress. Comp Biochem Physiol C 150:428–435
Xiang JH (2001) Disease occurrence and control strategies of mariculture organisms, vol 1–4. Ocean Press, Beijing, pp 78–83
Yu BP (1994) Cellular defenses against damage from reactive oxygen species. Physiol Rev 74:139–162
Zanotto FP, Whealthy M (1993) The effect of ambiant pH on electrolyte regulation during the postmoult period in freshwater crayfish Procambarus clarkii. J Exp Biol 178:1–19
Zhang QL, Li FH, Wang B, Zhang JQ, Liu YC, Zhou Q, Xiang JH (2007) The mitochondrial manganese superoxide dismutase gene in Chinese shrimp Fenneropenaeus chinensis: cloning, distribution and expression. Dev Comp Immunol 31:429–440
Zhou J, Wang WN, Ma GZ, Wang AL, He WY, Wang P, Liu Y, Liu JJ, Sun RY (2007) Gene expression of ferritin in tissues of the Pacific white shrimp, Litopenaeus vannamei after exposure to pH stress. Aquaculture 275:356–360
Acknowledgments
This research was supported by the National Natural Science Foundation of China (Grant nos. 30570287 and 30970455), and the Natural Science Foundation of the Guangdong Province in the P.R. China (Grant nos. 06025052 and 8151063101000035), and Guangdong Provincial Oceanic Fisheries Science and Technology Project (Grant no. A201001H02 and A200901H06). We are grateful for the help of Profs. Qili Feng and Sichun Zheng from the laboratory of Molecular Entomology, South China Normal University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, WN., Li, BS., Liu, JJ. et al. The respiratory burst activity and expression of catalase in white shrimp, Litopenaeus vannamei, during long-term exposure to pH stress. Ecotoxicology 21, 1609–1616 (2012). https://doi.org/10.1007/s10646-012-0937-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-012-0937-9