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A study on the effects of food quantity and quality on glutathione S-transferase (GST) activity and growth rate parameters of Daphnia carinata varying in age

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Abstract

The adverse influences of insufficient food and toxins on Daphnia carinata’s body growth, reproduction and tolerance were investigated in the laboratory. Different concentrations of Scendesmus obliquus and a mixture of S. obliquus and microcystin (MC)-containing Microcystis aeruginosa PCC7820 were used to feed D. carinata. Glutathione S-transferase (GST) activity towards five chemical compounds (substrates) was measured and used as an indicator of their tolerance. Body growth rate and clutch size of D. carinata decreased with declined concentration or decreased proportion of S. obliquus in the diet. GST activity decreased with ageing in D. carinata. However, GST activity to several chemical compounds increased when food quantity or food quality decreased. Adult D. carinata had a lower GST activity towards p-nitrophenenzyl chloride (PNBC) than juveniles and exhibited a sharp decline (P < 0.001) in GST activity towards PNBC as the animals aged. It is suggested that the age-specific decrease in GST activity is a possible mechanism for the high morality of adult D. carinata in the summer of eutrophic lakes.

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References

  • Baldwin WS, Leblanc GA (1996) Expression and induction of an immunochemically related class of Glutathione S-transferase in Daphnia magna. Comp Biochem Physiol 113:261–267

    Article  CAS  Google Scholar 

  • Benndorf J, Kranich J, Mehner T, Wagner A (2001) Temperature impact on the midsummer decline of Daphnia geleata: an analysis of long-term data from the biomanipulated Bautzen Reservoir (Germany). Freshw Biol 46(2):199–211

    Article  Google Scholar 

  • Best JH, Pflugmacher S, Wiegand C, Eddy FB, Metcalf JS, Codd GA (2002) Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione S-transferase activities in zebra fish (Danio rerio). Aquat Toxicol 60:223–231

    Article  CAS  PubMed  Google Scholar 

  • Boersma M, Van Tongeren OFR, Mooij WM (1996) Seasonal patterns in the mortality of Daphnia species in a shallow lake. Can J Fish Aquat Sci 53:18–28

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248

    Article  CAS  PubMed  Google Scholar 

  • Carmichael WW, Yu MJ, He JW, Yu JL (1988) Occurrence of the toxic cyanobacterium (blue-green algae) Microsystis aeruginosa in central China. Arch Hydrobiol 114(1):21–30

    Google Scholar 

  • Chen W, Song L, Ou D, Gan N (2005) Chronic toxicity and responses of several important enzymes in Daphnia magna on exposure to sublethal microcystin-LR. Environ Toxicol 20:323–330

    Article  CAS  PubMed  Google Scholar 

  • De Bernardi R (1974) The dynamics of a population of Daphnia hyalina Leydig in Lago Maggiore, Northern Italy. Mem Ist Ital Idrobiol 31:221–243

    Google Scholar 

  • DeMott WR (1999) Foraging strategies and growth inhibition in five daphnids feeding on mixture s of a toxic cyanobacterium and a green alga. Freshw Biol 42:263–274

    Article  Google Scholar 

  • DeMott WR, Kerfoot WC (1982) Competition among cladocerans: nature of the interaction between Bosmina and Daphnia. Ecology 63:1806–1825

    Article  Google Scholar 

  • Deng DG (2004) Ecological studies on the effects of eutrophication on plankton communities in a large shallow lake, Lake Chaohu. PhD Thesis, Institute of Hydrobiology, The Chinese Academy of Science, pp 137 (In Chinese with an English abstract)

  • Ferrão-Filho AS, Azevedo SMFO (2003) Effects of unicellular and colonial forms of toxic Microcystis aeruginosa from laboratory cultures and natural populations on tropical cladocerans. Aquat Ecol 37:23–35

    Article  Google Scholar 

  • Ferrão-Filho AS, Azevedo SMFO, DeMott WR (2000) Effects of toxic and non-toxic Cyanobacteria on the life history of tropical and temperate cladocerans. Freshw Biol 45:1–19

    Article  Google Scholar 

  • Fulton RS III, Paerl HW (1987a) Effects of colonial morphology on zooplankton utilization of algal resources during cyanobacterium algal (Microcystis aeruginosa) blooms. Limnol Oceanogr 32:634–644

    Article  Google Scholar 

  • Fulton RS III, Paerl HW (1987b) Toxic and inhibitory effects of the cyanobacterium algal Microcystis aeruginosa on herbivorous zooplankton. J Plankton Res 9:837–855

    Article  Google Scholar 

  • Gliwicz ZM, Ghilarov A, Pijanowska J (1981) Food and predation as major factors limiting two natural populations of Daphnia cucullata Sars. Hydrobiologia 80:205–218

    Article  Google Scholar 

  • Guo NC, Xie P (2006) Development of tolerance against toxic Microcystis aeruginosa in three cladocerans and the ecological implications. Environ Pollut 143:513–518

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson S, Hansson LA (2004) Development of tolerance against toxic Cyanobacteria in Daphnia. Aquat Ecol 38:37–44

    Article  Google Scholar 

  • Habdous M, Vincent-Viry M, Visvikis S, Siest G (2002) Rapid spectrophotometric method for serum glutathione S-transferases activity. Clin Chim Acta 326:131–142

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Jakoby MB (1981) Assays for differentiation of glutathione S-transferases. Meth Enzymol 77:398–405

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby MB (1974) Glutathione S-transferases. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Hayaoka T, Dauterman WC (1982) Induction of glutathione S-transferase by b-phenobabital and pesticides in various house fly strains and its effect on toxicity. Pest Biochem Physiol 17:113–119

    Article  CAS  Google Scholar 

  • Hovenkamp W (1989) Instar-dependent mortality rates of coexisting Daphnia species in Lake Vechten, the Netherlands. J Plankton Res 11:487–502

    Article  Google Scholar 

  • Hovenkamp W (1990) Instar-specific mortalities of coexisting Daphnia species in relation to food and invertebrate predation. J Plankton Res 12:483–495

    Article  Google Scholar 

  • Huang XF (1999) Survey, observation and analysis of lake ecology. Standards Press of China, Beijing

    Google Scholar 

  • Hülsmann S (2003) Recruitment patterns of Daphnia a key for understanding midsummer declines? Hydrobiologia 491:35–46

    Article  Google Scholar 

  • Hülsmann S, Weiler W (2000) Adult, not juvenile mortality as a major reason for the midsummer decline of Daphnia population. J Plankton Res 22:151–168

    Article  Google Scholar 

  • Lampert W (1981) Inhibitory and toxic effects of cyanobacterium algae on Daphnia. Hydrobiologia 66:285–298

    Google Scholar 

  • Lampert W (1986) Response of the respiratory rate of Daphnia magna to changing food conditions. Oecologia 70:495–501

    Article  Google Scholar 

  • Leblanc GA, Cochrane BJ (1985) Modulation of substrate-specific glutathione S-transferase activity in Daphnia magna with concomitant effects on toxicity tolerance. Comp Biochem Physiol 82c:37–42

    CAS  Google Scholar 

  • Leblanc GA, Hilgenberg B, Cochrane BJ (1988) Relationships between the structures of chlorinated phenols, their toxicity and their ability to induce glutathione S-transferase activity in Daphnia magna. Aquat Toxicol 12:147–156

    Article  CAS  Google Scholar 

  • Lürling M (2003) Effects of microcystin–free and microcystin-containing strains of the cyanobacterium Microsystis aeruginosa on growth of the grazer Daphnia magna. Environ Toxicol 18:202–210

    Article  PubMed  Google Scholar 

  • Lynch M (1989) The life history consequences of resource depression in Daphnia pulex. Ecology 70:246–256

    Article  Google Scholar 

  • Pflugmacher S, Wiegand C, Oberemm A, Beattie KA, Krause E, Codd GA, Steinberg CEW (1998) Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin–LR, the first step of detoxication. Biochem Biophys Acta 1425:527–533

    CAS  PubMed  Google Scholar 

  • Pflugmacher S, Wiegand C, Werner S, Schröder H, Kankaanpää H (2005) Activity and substrate specificity of cytosolic and microsomal glutathione S-transferase in australian black tiger prawns (Penaeus monodon) after exposure to cyanobacterial toxins. Environ Toxicol 20:301–307

    Article  CAS  PubMed  Google Scholar 

  • Pinho GLL, Rosa CMD, Yunes JS, Luquet CM, Bianchini A, Monserrat JM (2003) Toxic effects of microcystins in the hepatopancreas of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae). Comp Biochem Physiol Part C 135:459–468

    CAS  Google Scholar 

  • Reinikainen M, Hietala J, Walls M (1999) Reproductive allocation in Daphnia exposed to toxic Cyanobacteria. J Plankton Res 21:1553–1564

    Article  Google Scholar 

  • Repka S, Veen A, Vijverberg J (1999) Morphological adaptations in filtering screens of Daphnia galeata to food quantity and food quality. J Plankton Res 2:971–989

    Article  Google Scholar 

  • Sagara J, Sugita Y (2001) Characterization of cytosolic glutathione S-transferase in cultured Astrocytes. Brain Res 902:190–197

    Article  CAS  PubMed  Google Scholar 

  • Sen A, Semiz A (2007) Effects of metals and detergents on biotransformation and de -toxification enzymes of leaping mullet (Liza saliens). Ecotoxicol Environ Saf 68(3):405–411

    Article  CAS  PubMed  Google Scholar 

  • Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106:433–471

    Google Scholar 

  • Threlkeld ST (1979) The midsummer dynamics of two Daphnia species in Wintergreen Lake. Mich Ecol 60:165–179

    Google Scholar 

  • Trabeau M, Bruha-Keap R, McDemott C, Keomany M, Millsaps A, Emery A, Jr (2004) Midsummer decline of a Daphnia population attributed in part to cyanobacterial capsule production. J Plankton Res 26:949–961

    Google Scholar 

  • Vijverberg J (1976) The effect of food quantity and quality on the growth, birth-rate and longevity of Daphnia hyalina Leydig. Hydrobiologia 51:99–108

    Article  Google Scholar 

  • Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357:65–72

    Article  CAS  PubMed  Google Scholar 

  • Walls M, Laurēn-Määttä CL, Ketola M, Ohra-Aho P, Reinikainen MS, Repka S (1997) Phenotypic plasticity of Daphnia life history traits the roles of predation, food level and toxic Cyanobacteria. Freshw Biol 38:353–364

    Article  Google Scholar 

  • Wiegand C, Pflugmacher S, Oberemm A, Meems N, Beattie KA, Steinberg CEW, Codd GA (1999) Uptake and effects of microcystin-LR on detoxication enzymes of early life stages of the zebra fish (Danio rerio). Environ Toxicol 14:89–95

    Article  CAS  Google Scholar 

  • Zhao Y, Wang ZQ, Yang ZP, Xie CP, Fan Q, Wang Y (2002) Investigation on water pollution by algae at locations of water collection in Chaohu. J Environ Heal 19(4):316–318

    CAS  Google Scholar 

  • Zheng L, Xie P, Li YL, Yang H, Wang SB, Guo NC (2004) Variation of intracellular and extracellular microcystins in a shallow, hypereutrophic subtropical Chinese lake with dense cyanobacterial blooms. Bull Environ Contam Toxicol 73:698–706

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I am much indebted to Prof. Leblanc for providing me with a special custom-made version of the methods for analysing GST activities. I would like to thank Prof. Kong for discussing and correcting the manuscript. Min Zhang for greatly improving the English of an earlier draft of the manuscript and two anonymous referees, whose critical comment led to considerable improvement. This study was supported by the National Basic Research Programme of China (973 Programme, Grant No. 2008CB418101).

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Correspondence to Ping Xie.

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Handling Editor: R. D. Gulati.

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Guo, N., Xie, P. A study on the effects of food quantity and quality on glutathione S-transferase (GST) activity and growth rate parameters of Daphnia carinata varying in age. Aquat Ecol 45, 63–73 (2011). https://doi.org/10.1007/s10452-010-9324-x

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