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Antioxidant defense properties of Arctic amphipods: comparison between deep-, sublittoral and surface-water species

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Abstract

The toxic reactive oxygen species (ROS), produced naturally in an oxygenated environment, led to the development of antioxidant defenses by aerobic organisms to prevent tissue damage. Polar marine waters are regarded as a strongly prooxidant ecosystem, due to the high dissolved oxygen level and intense UV radiation during summer, while the deep waters are considered refuges against oxidative stress. In order to further elucidate the prooxidant and antioxidant forces associated with cold-water ecosystems and the implications of UV radiation, we sampled three amphipod species living at three different depths in the same water mass of the Arctic Ocean, characterized by low temperature (ca. 0°C), high oxygen level, and high ROS concentration in the surface water. The three species were the deep-sea amphipod Eurythenes gryllus, the benthic sublittoral amphipod Anonyx nugax and the surface-water species Gammarus wilkitzkii inhabiting the ice pack. The total oxyradical scavenging capacity (TOSC) was measured in the cytosolic fraction of the digestive gland and in the cell-free hemolymph of the three amphipod species. A significantly low TOSC toward peroxyl and peroxynitrite radicals (P<0.05) in E. gryllus compared with the shallow-water species (A. nugax) can be explained by the low metabolism of the deep-sea species. In the cell-free hemolymph, TOSC values are similar between E. gryllus and A. nugax, while in G. wilkitzkii a lower and higher TOSC toward hydroxyl and peroxynitrite, respectively, indicate specific adaptation to oxidative stress. Experimental exposure of A. nugax and G. wilkitzkii to H2O2 resulted in a significant change in TOSC (P<0.05) measured in the digestive gland and in the cell-free hemolymph of A. nugax, while no change (P>0.05) was noted in G. wilkitzkii. These data suggest that A. nugax is highly susceptible to oxidative stress and that G. wilkitzkii is characterized by a mechanism that prevents the diffusion of exogenous ROS through the gills or allows excretion of internal H2O2 through the gills to the environment.

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References

  • Aarset AV (1991) The ecophysiology of under-ice fauna. Polar Res 10:309–324

    Google Scholar 

  • Bell KL, Smith VJ (1994) Occurrence and distribution of antioxidant enzymes in the hemolymph of the shore crab Carcinus maenas. Mar Biol 123:829–836

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Analyt Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Britton JC, Morton B (1994) Marine carrions and scavengers. Oceanogr Mar Biol Annu Rev 32:369–434

    Google Scholar 

  • Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10:30–36

    Article  Google Scholar 

  • Cooper WJ, Shao CW, Lean DRS, Gordon AS, Scully FE (1994) Factors affecting the distribution of H2O2 in surface waters environmental chemistry of lakes and reservoirs. Adv Chem Ser 237:391–422

    CAS  Google Scholar 

  • DiGiulio RT, Washburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxicol Chem 8:1103–1123

    CAS  Google Scholar 

  • Duquesne S, Liess M (2003) Increased sensitivity of the macroinvertebrate Paramorea walkeri to heavy-metal contamination in the presence of solar UV radiation in Antarctic shoreline waters. Mar Ecol Prog Ser 255:183–191

    CAS  Google Scholar 

  • Estevez MS, Malanga G, Puntarulo S (2001) UV-B effects on Antarctic Chlorella sp. cells. J Photochem Photobiol B Biol 62:19–25

    Article  CAS  Google Scholar 

  • Gieseg SP, Cuddihy S, Jonathan VH, Davison W (2000) A comparison of plasma vitamin C and E levels in two Antarctic and two temperate water fish species. Comp Biochem Physiol B 125:371–378

    Article  CAS  PubMed  Google Scholar 

  • Heise K, Puntarulo S, Pörtner HO, Abele D (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp Biochem Physiol C Comp Pharmacol Toxicol 134:79–90

    Article  CAS  Google Scholar 

  • Janssens BJ, Childress JJ, Baguet F, Rees JF (2000) Reduced enzymatic antioxidative defence in deep-sea fish. J Exp Biol 203:3717–3725

    CAS  PubMed  Google Scholar 

  • Legeżyńska J, Weslawski JM, Presler P (2000) Benthic scavengers collected by baited traps in the high Arctic. Polar Biol 23:539–544

    Article  Google Scholar 

  • Lønne OJ, Gulliksen B (1991) Sympagic macro-fauna from multiyear sea-ice near Svalbard. Polar Biol 11:471–477

    Google Scholar 

  • Opalinski KW, Weslawski JM (1989) Oxygen consumption in Arctic amphipods: metabolic cold compensation. In: Klekowski RZ, Jurewicz-Styczynzka E, Falkowski L (eds) Proceedings of the 21st Eur Mar Biol Symp. Ossolineum, Wroclaw, pp 137–142

  • Premke K, Muyakshin S, Klages M, Wegner J (2003) Evidence for long-range chemoreceptive tracking of food odour in deep-sea scavengers by scanning sonar data. J Exp Mar Biol Ecol 285/286:283–294

    Google Scholar 

  • Qian JG, Mopper K, Kieber DJ (2001) Photochemical production of the hydroxyl radical in Antarctic waters. Deep-Sea Res Part I 48:741–759

    Google Scholar 

  • Regoli F, Winston GW (1999) Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals and hydroxyl radicals. Toxicol Appl Pharmacol 156:96–105

    Article  CAS  PubMed  Google Scholar 

  • Regoli F, Principato GB, Bertoli E, Nigro M, Orlando E (1997) Biochemical characterization of the antioxidant system in the scallop Adamussium colbecki, a sentinel organism for monitoring the Antarctic environment. Polar Biol 17:251–258

    Article  Google Scholar 

  • Regoli F, Nigro M, Bompadre S, Winston G (2000a) Total oxidant scavenging capacity (TOSC) of microsomal and cytosolic fractions from Antarctic, Arctic and Mediterranean scallops: differentiation between three potent oxidants. Aquat Toxicol 49:13–25

    Article  CAS  PubMed  Google Scholar 

  • Regoli F, Nigro M, Chiantore M, Gorbi S, Winston G (2000b) Total oxidant scavenging capacity of Antarctic, Arctic, and Mediterranean scallops. Ital J Zool 67:85–94

    CAS  Google Scholar 

  • Regoli F, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S, Winston GW (2002a) Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Mar Environ Res 54:419–423

    Article  CAS  PubMed  Google Scholar 

  • Regoli F, Nigro M, Chiantore M, Winston GW (2002b) Seasonal variations of susceptibility to oxidative stress in Adamussium colbecki, a key bioindicator species for the Antarctic marine environment. Sci Total Environ 289:205–211

    Article  CAS  PubMed  Google Scholar 

  • Rubach S, Sundet J (1987) Ressurskartlegging av haneskjell (Chlamys islandica (O. F. Müller)) ved Jan Mayen og i Svalbardsonen. Skriftserie fra Institutt for Fiskerifag, Serie B: Ressursbiologi

  • Sainte-Marie B (1992) Foraging of scavenging deep-sea lysianassoid amphipods. In: Rowe GT, Pariente V (eds) Deep-sea food chains and the global carbon cycle. Kluwer, Amsterdam, pp 105–124

  • Schulz A, Rex M, Harris NRP, Braathern GO, Reimer E, Alfier R, Kilbane-Dawe I, Eckermann S, Allaart M, Alpers M, Bojkov B, Cisneros J, Claude H, Cuevas E, Davies J, De Backer H, Dier H, Dorokhov V, Fast H, Godin S, Johnson B, Kois B, Kondo Y, Kosmidis E, Kyro E, Litynska Z, Mikkelsen IS, Molyneux MJ, Murphy G, Nagai T, Nakane H, O’Connor F, Parrondo C, Schmidlin FJ, Skrivankova P, Varotsos C, Vialle C, Viatte P, Yushkov V, Zerefos C, von der Gathen P (2001) Arctic ozone loss in threshold conditions: match observations in 1997/1998 and 1998/1999. J Geophys Res Atmos 106:7495–7503

    Article  CAS  Google Scholar 

  • Scully NM, McQueen DJ, Lean DRS, Cooper WJ (1996) Hydrogen peroxide formation: the interaction of ultraviolet radiation and dissolved organic carbon in lake waters along a 43–75 degrees N gradient. Limnol Oceanogr 41:540–548

    CAS  Google Scholar 

  • Stolarski R, Bojkov R, Bishop L, Zerefos C, Staehelin J, Zawodny J (1992) Measured trends in ozone. Science 256:342–349

    CAS  Google Scholar 

  • Takeuchi I, Watanabe K (1998) Respiration and swimming speed of the necrophageous amphipod Eurythenes gryllus from Antarctic deep waters. Mar Ecol Prog Ser 163:285–288

    Google Scholar 

  • Viarengo A, Abele-Oeschger D, Burlando B (1998) Effects of low temperature on prooxidant processes and antioxidant defence systems in marine organisms. In: Pörtner HO, Playle RC (eds) Cold ocean physiology. Society for Experimental Biology Seminar Series 66, Cambridge University Press, Cambridge

  • Werner I, Gradinger R (2002) Under-ice amphipods in the Greenland Sea and Fram Strait (Arctic): environmental controls and seasonal patterns below the pack ice. Mar Biol 140:317–326

    Article  Google Scholar 

  • Werner I, Auel H, Friedrich C (2002) Carnivorous feeding and respiration of the Arctic under-ice amphipod Gammarus wilkitzkii. Polar Biol 25:523–530

    Article  Google Scholar 

  • Weslawski JM, Opalinski KW (1997) Winter and summer metabolic rates of Arctic amphipods. Preliminary results. In: Glowacki P (ed) Polish polar studies: 24th polar symposium. Institute of Geophysics of the Polish Academy of Sciences, Warszawa, pp 307–317

  • Whiteley NM, Taylor EW, ElHaj AJ (1996) A comparison of the metabolic cost of protein synthesis in stenothermal and eurythermal isopod crustaceans. Am J Physiol 40:1295–1303

    Google Scholar 

  • Wilhelm D, Gonzaleaflecha B, Boveris A (1994) Gill diffusion as a physiological mechanism for hydrogen-peroxide elimination by fish. Braz J Med Biol Res 27:2879–2882

    PubMed  Google Scholar 

  • Winston GW, DiGiulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–191

    Article  CAS  Google Scholar 

  • Winston GW, Moore NM, Kirchin MA, Soverchia C (1996) Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: lysosomal localization and effect of xenobiotics. Comp Biochem Physiol C 113:221–229

    Article  CAS  PubMed  Google Scholar 

  • Winston GW, Regoli F, Dugas AJ, Fong JH, Blanchard KA (1998) A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Radic Biol Med 24:480–493

    Article  CAS  PubMed  Google Scholar 

  • Yocis BH, Kieber DJ, Mopper K (2000) Photochemical production of hydrogen peroxide in Antarctic waters. Deep-Sea Res Part I 47:1077–1099

    Google Scholar 

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Acknowledgements

The authors are grateful to the crew of the R.V. “Jan Mayen” from the University of Tromsø. This study was financed by the Norwegian Research Council under the program “Marine Resource, Environment and Management” (project no. 146478/120) and by the Norwegian marine research laboratory RF-Akvamiljø.

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Correspondence to L. Camus.

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Communicated by M. Kühl, Helsingør

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Camus, L., Gulliksen, B. Antioxidant defense properties of Arctic amphipods: comparison between deep-, sublittoral and surface-water species. Marine Biology 146, 355–362 (2005). https://doi.org/10.1007/s00227-004-1424-5

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  • DOI: https://doi.org/10.1007/s00227-004-1424-5

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