Skip to main content

Advertisement

SpringerLink
Log in

The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Hydrothermal vents are a unique environment of extreme physical–chemical characteristics and biological species composition. Cd is a toxic non-essential metal present in high concentrations in the hydrothermal vent environment, contrary to those found in marine coastal areas. Cd toxicity has been related, among other things, with reactive oxygen species production, even though this is a non-redox metal. Bathymodiolus azoricus is a deep-sea Mytilid bivalve very common in the Mid Atlantic Ridge (MAR) hydrothermal vent fields and very little is known about the antioxidant defence system in this specie. Because lethal Cd concentration in B. azoricus is unknown, the aim of this study was to assess the effects of a Cd concentration higher than that found in the hydrothermal vents on oxidative stress biomarkers, such as antioxidant enzymes. Mussels were exposed to 100 μg l−1 Cd during 24, 48 and 144 h, respectively, in a pressurized aquarium (IPOCAMP). Superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (GPx), total oxyradical scavenging capacity (TOSC), metallothionein (MT) and lipid peroxidation (LPO) were measured in the gills and mantle of B. azoricus. The results indicate that gills are first affected by Cd toxicity. This may be due to different physiological functions of the tissues and by the presence of thio and methanotrophic symbiotic bacteria in the gills. The SOD and CAT are inhibited during the first day of exposure in the gills, although TOSC and MT concentrations were the same in control and exposed mussels. In the mantle, enzymatic activation only occurred after 6 days, and no significant differences in MT concentrations were found in the control and exposed mussels during the first day, as observed in the gills.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bebianno MJ, Company RM, Serafim AM, Camus L, Cosson R, Fiala-Medioni A Antioxidant enzymes and lipid peroxidation in Bathymodiolus azoricus from Middle Atlantic Ridge Thermal Vent Fields. Aquat Toxicol (in press)

  • Bebianno MJ, Langston WJ (1991) Metallothionein induction in Mytilus edulis exposed to cadmium. Mar Biol 108(1):91–96

    Article  CAS  Google Scholar 

  • Bebianno MJ, Langston WJ (1992) Cadmium induction of metallothionein synthesis in the Mytilus galloprovincialis. Comp Biochem Physiol C 103:79–85

    Article  Google Scholar 

  • Bebianno MJ, Nott JA, Langston WJ (1993) Cadmium metabolism in the clam Ruditapes decussata: the role of metallothioneins. Aquat Toxicol 27:315–334

    Article  CAS  Google Scholar 

  • Bebianno MJ, Serafim MA (1998) Comparison of metallothionein induction in response to cadmium in the gills of the bivalve molluscs Mytilus galloprovincialis and Ruditapes decussatus. Sci Total Environ 214:123–131

    Article  CAS  Google Scholar 

  • Bebianno MJ, Serafim MA, Rita MF (1994) Involvement of metallothionein in cadmium accumulation and elimination in the clam Ruditapes decussata. Bull Environ Contam Toxicol 53:726–732

    Article  CAS  Google Scholar 

  • Beyersmann D, Hechtenberg S (1997) Cadmium, gene regulation and cellular signaling in mammalian cells. Toxicol Appl Pharmacol 144:247–261

    Article  CAS  Google Scholar 

  • Blum J, Fridovich I (1984) Enzymatic defences against oxygen toxicity in the hydrothermal vent animals Riftia pachyptila and Calyptogena magnifica. Arch Biochem Biophys 228(2):617–620

    Article  CAS  Google Scholar 

  • Caccia VG, Millero FJ, Palanques A (2003) The distribution of trace metals in Florida Bay sediments. Mar Pollut Bull 46:1420–1433

    Article  CAS  Google Scholar 

  • Camus L, Birkely SR, Jones MB, Børseth JF, Grøsvik BE, Gulliksen B, Lønne OJ, Regoli F, Depledge MH (2003) Biomarker responses and PAH uptake in Mya truncata following exposure to oil-contaminated sediment in an Arctic fjord (Svalbard). Sci Total Environ 308:221–234

    Article  CAS  Google Scholar 

  • Camus L, Jones MB, Børseth JF, Regoli F, Depledge MH (2002a) Heart rate, respiration and total oxyradical scavenging capacity of the Arctic spider crab, Hyas araneus, following exposure to polycyclic aromatic compounds via sediment and injection. Aquat Toxicol 60:1–13

    Article  Google Scholar 

  • Camus L, Jones MB, Børseth JF, Grøsvik BE, Regoli F, Depledge MH (2002b) Total oxyradical scavenging capacity and cell membrane stability of haemocytes of the Arctic scallop, Chlamys islandicus, following benzo(a)pyrene exposure. Mar Environ Res 54:425–430

    Article  CAS  Google Scholar 

  • Cheeseman KM (1982) Effects of scavengers and inhibitors on lipid peroxidation in rat liver microsomes. In: MacBrien DC, Slater TF (eds) Free radicals, lipid peroxidation and cancer. Academic Press, New York, pp 196–211

    Google Scholar 

  • Cheeseman KH, Slater TF (1993) An introduction to free radical biochemistry. Br Med Bull 49(3):481–493

    Article  CAS  Google Scholar 

  • Company R, Serafim A, Bebianno MJ, Cosson R, Shillito B, Fiala-Médioni A (2004) Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 58:377–381

    Article  CAS  Google Scholar 

  • Cosson R (1997) Adaptation des organismes hydrothermaux à la contrainte métallique. Bull Soc Zoo Fr 122(2):109–126

    Google Scholar 

  • Cosson-Mannevy MA, Cosson RP, Gaill F, Laubier L (1988) Transfert, accumulation et regulation des elements minéraux chez les organismes des sources hydrothermales. Oceanol Acta 8:219–226

    Google Scholar 

  • Cosson RP, Vivier J (1997) Interactions of metallic elements and organisms within hydrothermal vents. Cah Biol Mar 38:43–50

    Google Scholar 

  • Desbruyères D, Almeida A, Biscoito M, Comtet T, Khripounoff N, Le Bris N, Sarradin PM, Segonzac M (2000) A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: dispersal vs. environmental controls. Hydrobiologia 440:201–216

    Article  Google Scholar 

  • Desbruyères D, Biscoito M, Caprais JC, Colaço A, Comtet T, Crassous P, Fouquet Y, Khripounoff A, Le Bris N, Olu K, Riso R, Sarradin PM, Segonzac M, Vangriesheim A (2001) Variations in deep-sea hydrothermal vent communities in the Mid-Atlantic Ridge near the Azores plateau. Deep-Sea Res Part I 48:1325–1346

    Article  Google Scholar 

  • Dixon DR, Pruski AM, Dixon LRJ (2004). The effects of hydrostatic pressure change on DNA integrity in the hydrothermal-vent mussel Bathymodiolus azoricus: implications for future deep-sea mutagenicity studies. Mutat Res 552(1–2):235–246

    Article  CAS  Google Scholar 

  • Domouhtsidou GP, Dailianis S, Kaloyianni M, Dimitriadis VK (2004) Lysosomal membrane stability and metallothionein content in Mytilus galloprovincialis (L.), as biomarkers combination with trace metal concentrations. Mar Pollut Bull 48:572–586

    Article  CAS  Google Scholar 

  • Douville E, Charlou JL, Oelkers EH, Bienvenu P, Jove Colon CF, Donval JP, Fouquet Y, Prieur D, Appriou P (2002) The rainbow vent fluids (36°14′N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids. Chem Geol 184:37–48

    Article  CAS  Google Scholar 

  • EPA (2001) Update of ambient water criteria for cadmium. U.S. environmental Protection Agency Office of Water. Office of Science and Technology, Washington, DC

  • Erdelmeier I, Gerard-Monnier D, Yadan JC, Acudiere J (1998) Reactions of N-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Mechanistic aspects of the colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1184–1194

    Article  CAS  Google Scholar 

  • Fiala-Médioni A, McKiness ZP, Dando P, Boulegue J, Mariotti A, Alayse-Danet AM, Robinson JJ, Cavanaugh C (2002) Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Mar Biol 141:1035–1043

    Article  Google Scholar 

  • Fridovich IA (1978) The biology of oxygen radicals. Science 201:875–880

    Article  CAS  Google Scholar 

  • Geret F, Serafim A, Barreira L, Bebianno MJ (2002a) Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus. Biomarkers 7(3):242–256

    Article  CAS  Google Scholar 

  • Geret F, Jouan A, Turpin V, Bebianno MJ, Cosson R (2002b) Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve molluscs: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquat Living Resour 15:61–66

    Article  Google Scholar 

  • Geret F, Rousse N, Riso R, Sarradin PM, Cosson RP (1998) Metal compartmentalization and metallothionein isoforms in mussels from Mid-Atlantic Ridge; preliminary approach to fluid-organism relationship. Cah Biol Mar 39:291–293

    Google Scholar 

  • Giguère A, Couillard Y, Campbell PGC, Perceval O, Hare L, Pinel-Alloul B, Pellerin J (2003) Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquat Toxicol 64:85–200

    Article  Google Scholar 

  • Greenwald RA (1985) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, FL

    Google Scholar 

  • Hartwig A (1994) Role of DNA repair inhibition in lead and chromium-induced genotoxicity: a review. Environ Health Perspect 102:45–50

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassoun EA, Stohs SJ (1996) Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology 112(2–3):219–226

    Article  CAS  Google Scholar 

  • Hussein T, Shukla GS, Chandra SV (1987) Effects of cadmium on superoxide dismutase and lipid peroxidation in liver and kidney of growing rats: in vivo and vitro studies. Pharmacol Toxicol 60:355–358

    Article  Google Scholar 

  • Kochevar RE, Childress JJ, Fisher CR, Minnich E (1992) The methane mussel: roles of symbiont and host in the metabolic utilization of methane. Mar Biol 112:389–401

    Article  CAS  Google Scholar 

  • Kumar R, Asic K, Agarwal K, Seth PK (1996) Oxidative stress-mediated neurotoxicity of cadmium. Toxicol Lett 89:65–69

    Article  CAS  Google Scholar 

  • Langston WJ (1990) Toxic effects of metals and the incidence of metal pollution in marine ecosystems. In: Furness RW, Rainbow PS (eds) Heavy metal levels in marine environment. CRC Press, Boca Raton, FL

    Google Scholar 

  • Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958

    Article  CAS  Google Scholar 

  • Lecoeur S, Videmann S, Berny Ph (2004) Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dreissena polymorpha. Environ Res 94:184–191

    Article  CAS  Google Scholar 

  • León AM, Palma JM, Corpas FJ, Gómez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Rio LA, Sandalio LM (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820

    Article  Google Scholar 

  • Lowell RP, Rona PA, Von Herzen PR (1995) Seafloor hydrothermal systems. J Geophys Res B100:327–352

    Article  Google Scholar 

  • Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Manca D, Richard AC, van Tra H, Chevalier G (1994) Relation between lipid peroxidation and inflammation in the pulmonary toxicity of cadmium. Arch Toxicol 68:364–369

    Article  CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055

    CAS  PubMed  Google Scholar 

  • Muller L (1991) Consequences of cadmium toxicity in rat hepatocytes, mitochondrial dysfunction and lipid peroxidation. Toxicology 40:285–292

    Article  Google Scholar 

  • Nelson DC, Hagen KD, Edwards DB (1995) The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium. Mar Biol 121:487–495

    Article  Google Scholar 

  • Okamoto OK, Pinto E, Latorre LR, Bechara EJH, Colepicolo P (2001) Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Contam Toxicol 40:18–24

    Article  CAS  Google Scholar 

  • Olafson RW, Sim RG (1979) An electrochemical approach to quantification and characterization of metallothioneins. Anal Biochem 100:343–351

    Article  CAS  Google Scholar 

  • Prusky AM, Dixon DR (2002) Effects of cadmium on nuclear integrity and DNA repair efficiency in the gill cells of Mytilus edulis L. Aquat Toxicol 57:127–137

    Article  Google Scholar 

  • Regoli F (2000) Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat Toxicol 50:351–361

    Article  CAS  Google Scholar 

  • Regoli F, Nigro M, Bompadre S, Winston GW (2000) 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  Google Scholar 

  • Regoli F, Winston GW (1998) Applications of a new method for measuring the total oxyradical scavenging capacity in marine invertebrates. Mar Environ Res 46(1–5):439–442

    Article  CAS  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  Google Scholar 

  • Regoli F, Winston GW, Mastrangelo V, Principato G, Bompadre S (1998) Total oxidant scavenging capacity in mussel Mytilus sp. as a new index of biological resistance to oxidative stress. Chemosphere 37(14–15):2773–2783

    CAS  Google Scholar 

  • Roesijadi G, Crecelius EA (1984) Elemental composition of the hydrothermal vent clam Calyptogena magnifica from the East Pacific Rise. Mar Biol 83:155–161

    Article  CAS  Google Scholar 

  • Roesijadi G, Klerks PL (1989) Kinetic analysis of cadmium binding to metallothionein and other intracellular ligands in oyster gills. J Exp Zool 251:1–12

    Article  CAS  Google Scholar 

  • Roesijadi G, Young JS, Crecelius EA, Thomas LE (1985) Distribution of trace metals in the hydrothermal vent clam Calyptogena magnifica. Bull Biol Soc Wash 6:311–324

    Google Scholar 

  • Rómeo M, Gnassia-Barelli M (1997) Effect of heavy metals on lipid peroxidation in the mediterranean clam Rudipates decussatus. Comp Biochem Physiol C 118(1):33–37

    Google Scholar 

  • Rousse N, Boulegue J, Cosson RP, Fiala-Medioni A (1998) Bioaccumulation des métaux chez le mytilidae hydrothermal Bathymodiolus sp. De la ride médio-atlantique. Oceanologica Acta 21(4):597–607

    Article  CAS  Google Scholar 

  • Sarradin PM, Caprais JC, Briand P, Gaill F, Shillito B, Desbruyeres D (1998) Chemical and thermal description of the environment of the Genesis hydrothermal vent community (13°N, EPR). Cah Biol Mar Roscoff 38:159–167

    Google Scholar 

  • Sarradin PM, Desbruyères D, Dixon DR, Almeida A, Caprais JC, Colaço A, Company R, Cosson R, Cueff V, Dando PR, Etoubleau J, Fiala-Médioni A, Gaill F, Godfroy A, Gwynn JP, Hourdez S, Jollivet D, Khripounoff A, Lallier F, Laulier M, Le Bris N, Martins I, Mestre N, Pruski AM, Rodier P, Santos RS, Shillito B, Zal F, Zbinden M (2001) ATOS cruise R/V l’Atalante, ROV Victor, June 22nd–July 21st 2001. InterRidge News 10(2):18–20

    Google Scholar 

  • Serafim MA, Company RM, Bebianno MJ, Langston WJ (2002) Effect of temperature and size on metallothionein synthesis in the gill of Mytilus galloprovincialis exposed to cadmium. Mar Environ Res 54:361–365

    Article  CAS  Google Scholar 

  • Shillito B, Jollivet D, Sarradin PM, Rodier P, Lallier FH, Desbruyères D, Gaill F, (2001) Temperature resistance of Hesiolyra bergi, a polychaetous annelid living on deep-sea vent smoker walls. Mar Ecol Prog Ser 216:141–149

    Article  Google Scholar 

  • Smith DR, Flegal AR (1989) Elemental concentrations of hydrothermal vent organisms from the Galapagos Rift. Mar Biol 102:127–133

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 8(2):321–336

    Article  Google Scholar 

  • Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2001) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 20:77–88

    Article  CAS  Google Scholar 

  • Thompson JAJ, Cosson RP (1984) An improved electrochemical method for the quantification of metallothionein in marine organisms. Mar Environ Res 11:137–152

    Article  CAS  Google Scholar 

  • Viarengo A, Canesi L, Pertica M, Poli G, Moore MN, Orunesu M (1990) Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis LAM. Comp Biochem Physiol C 97:37–42

    Article  Google Scholar 

  • Von Damm KL (1990) Seafloor hydrothermal activity: black smoker chemistry and chimneys. Annu Rev Earth Planet Sci 18:173–204

    Article  Google Scholar 

  • Von Damm KL, Oosting SE, Kozlowsky R, Buttermore LG, Colodner DC, Edmonds H, Edmond JM, Grebmeir JM (1995) Evolution of seafloor hydrothermal vent fluids at 9°54.5′N, EPR following a volcanic eruption. Nature 375:47–50

    Article  Google Scholar 

  • Watanabe M, Henmi K, Ogawa K, Suzuki T (2003) Cadmium-dependent generation of reactive oxygen species and mitochondrial DNA breaks in photosynthetic and non-photosynthetic stains of Euglena gracilis. Comp Biochem Physiol C 134:227–234

    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(3):480–493

    Article  CAS  Google Scholar 

  • Wu F, Zhang G, Dominy P (2003) Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environ Exp Bot 50:67–78

    Article  CAS  Google Scholar 

  • Yamada H, Miyahara T, Sasaki Y (1993) Inorganic cadmium increases the frequency of chemically induced chromosome aberrations in cultured mammalian cells. Mutat Res 302(3):137–145

    Article  CAS  Google Scholar 

  • Yang CF, Shen HM, Shen Y, Zhuang ZX, Ong CN (1997) Cadmium-induced oxidative cellular damage in human fetal lung fibroblasts (MRC-5 cells). Environ Health Perspect 105:712–716

    Article  CAS  Google Scholar 

  • Zhong Z, Troll W, Koenig KL, Frenkel K (1990) Carcinogenic sulfide salts of nickel and cadmium induce H2O2 formation by human polymorphonuclear leukocytes. Cancer Res 50:7570

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank P.M. Sarradin, chief scientist of ATOS cruise and D.R. Dixon, VENTOX project coordinator. The R.M. Company was financed by Fundação para a Ciência e a Tecnologia (grant SFRH/BD/904/2000) of the Ministry of Science and Technology of Portugal. This work was mainly funded by the EU Framework 5 Programme, Contract No. EVK3-CT1999-00003 VENTOX) and additional funding was provided 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.

Author information

Authors and Affiliations

  1. CIMA, Faculty of Marine and Environmental Sciences, University of Algarve, Campus de Gambelas, 8000, Faro, Portugal

    Rui Company, Angela Serafim & Maria João Bebianno

  2. ISOMer—UPRES-EA 2663, Laboratoire de Biologie Marine, Faculté des Sciences et Techniques, Université de Nantes, BP 92208, 44322, Nantes, France

    Richard Cosson

  3. The University Centre on Svalbard, PB 156, 9170, Longyearbyen, Norway

    Lionel Camus

  4. Akvamiljø as, Mekjarvik 12, 4070, Randaberg, Norway

    Lionel Camus

  5. Equipe Adaptations et Evolution en Milieux Extremes, UPMC-CNRS UMR 7138, 7 Quai St-Bernard, 75005, Paris, France

    Bruce Shillito

  6. Observatoire Océanologique, Université P.M. Curie, BP 44, 66651, Banyuls sur Mer, France

    Aline Fiala-Médioni

Authors
  1. Rui Company
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Serafim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard Cosson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lionel Camus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruce Shillito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aline Fiala-Médioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maria João Bebianno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria João Bebianno.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Company, R., Serafim, A., Cosson, R. et al. The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus . Marine Biology 148, 817–825 (2006). https://doi.org/10.1007/s00227-005-0116-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0116-0

Keywords

Search

Navigation