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Cadmium and copper toxicity in three marine macroalgae: evaluation of the biochemical responses and DNA damage

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Abstract

Marine macroalgae have evolved a different mechanism to maintain physiological concentrations of essential metal ions and non-essential metals. The objective of the present work was to evaluate the antioxidant response and DNA damage of copper and cadmium ions in three halophytes, namely, Acanthophora spicifera, Chaetomorpha antennina, and Ulva reticulata. Accumulation of copper was significantly higher (P < 0.05) than that of cadmium. Biochemical responses showed that copper was considerably more toxic than cadmium (P < 0.05). Decreases in glutathione content and fluctuations of super oxide dismutase, catalase, and glutathione peroxidase activities were observed corresponding to time and concentration of exposure. Interestingly, it was also observed that antioxidant levels decreased as a result of metal accumulation, which may be due to free radicals generated by copper and cadmium in seaweeds. The present study also showed that copper and cadmium increased oxidative stress and induced antioxidant defense systems against reactive oxygen species. The order of toxicity for metals in the studied seaweeds was U. reticulata > A. spicifera > C. antennina. DNA damage index analysis supported that copper was significantly (P < 0.05) more toxic than cadmium. Bioaccumulation, biochemical responses, and DNA damage observed in the here analyzed marine macroalgae after exposure to selected metals indicate that these marine organisms represent useful bioindicators of marine pollution.

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References

  • Achard-Joris M, Moreau JL, Lucas M, Baudrimont M, MesmerDudons N, Gonzalez P, Boudou A, Bourdineaud JP (2007) Role of metallothioneins in superoxide radical generation during copper redox cycling: defining the fundamental function of metallothioneins. Biochimie 89:1474–1488

    Article  CAS  Google Scholar 

  • Akcali I, Kucuksezgin F (2011) A biomonitoring study: heavy metals in macroalgae from eastern Aegean coastal areas. Mar Pollut Bull 62:637–645

    Article  CAS  Google Scholar 

  • Archana Devi C, Kumaraguru AK (2008) Toxicity of metals copper and cadmium on the brown macroalgal species of Pudumadam coast, Gulf of Mannar. Seaweed Res Utl 30:203–211

    Google Scholar 

  • Aslan M, Unlü MY, Türkmen N, Yilmaz YZ (2003) Sorption of cadmium and effects on growth, protein content, and photosynthetic pigment composition of Nasturtium officinale R. Br. and Mentha aquatica L. Bull Environ Contam Toxicol 71:323–329

    Article  CAS  Google Scholar 

  • Bajguz A (2010) An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under metals stress. Environ Exp Bot 68:175–179

    Article  CAS  Google Scholar 

  • Bajguz A, Godlewska-Żyłkiewicz B (2004) Protective role of 20-hydroxyecdysone against lead stress in Chlorella vulgaris cultures. Phytochemistry 65:711–720

    Article  CAS  Google Scholar 

  • Baumann HA, Morrison L, Stengel DB (2009) Metal accumulation and toxicity measured by PAM—chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol Environ Saf 72:1063–1075

    Article  CAS  Google Scholar 

  • Bermúdez YG, Rodrígues IL, Bermúdez OG, Guibal E (2011) Nickel biosorption using Gracilaria caudata and Sargassum muticum. Chem Eng J 166:122–131

    Article  Google Scholar 

  • Boyne AF, Ellman GL (1972) A methodology for analysis of tissue sulfhydryl components. Anal Biochem 46:639–653

    Article  CAS  Google Scholar 

  • Burrit DJ, Larkindale J, Hurd K (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838

    Article  Google Scholar 

  • Carrillo Domínguez S, Casas Valdez M, Ramos Ramos F, Pérez-Gil F, Sánchez-Rodríguez I (2002) Algas marinas de Baja California Sur, México: valor nutricional. Arch Latinoam Nutr 52:400–405

    Google Scholar 

  • Chan SM, Wang W, Ni I (2003) The uptake of Cd, Cr, and Zn by the macroalga Enteromorpha crinita and subsequent transfer to the marine herbivorous rabbitfish, Sigunus canaliculatus. Arch Environ Contam Toxicol 44:298–306

    Article  CAS  Google Scholar 

  • Collén JE, Pinto M, Pedersen, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutants metals. Arch Environ Contam Toxicol 45:337–342

    Article  Google Scholar 

  • Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins—new functions and new insights into specificity. J Biol Chem 278:23747–23752

    Article  CAS  Google Scholar 

  • Contreras L, Moenne A, Correa JA (2005) Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper enriched coastal environments. J Phycol 41:1184–1195

    Article  CAS  Google Scholar 

  • Das K, Samanta L, Chainy GBN (2000) A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals. Indian J Biochem Biophys 37:201–204

    CAS  Google Scholar 

  • Dawes CJ (1998) Marine Botany. Wiley and Sons, Inc., New York, p 480

    Google Scholar 

  • De Vos RCH, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper‐induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858

    Article  Google Scholar 

  • Dhargalkar VK, Neelam P (2005) Seaweed: promising plant of the millennium. Sci Cult 71:60–66

    Google Scholar 

  • Grasshoff K, Ehrdardt M, Kremling K, Anderson LG (1999) Methods of seawater analysis. Wiley

  • Groppa MD, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. Biometals 20:185–195

    Article  CAS  Google Scholar 

  • Gupta V, Kumar M, Kumari P, Reddy CRK, Jha B (2011) Optimization of protoplast yields from the red algae Gracilaria dura (C. Agardh) J. Agardh and G. verrucosa (Huds.) Papenfuss. J Appl Phycol 23:209–218

    Article  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press Oxford, United Kingdom

    Google Scholar 

  • Han T, Choi GW (2005) A novel marine algal toxicity bioassay based on sporulation inhibition in the green macroalga Ulva pertusa (Chlorophyta). Aquat Toxicol 75:202–212

    Article  CAS  Google Scholar 

  • Hegedus A, Erdei S, Horvath G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  CAS  Google Scholar 

  • Huang X, Ke C, Wang WX (2010) Cadmium and copper accumulation and toxicity in the macroalga Gracilaria tenuistipitata. Aquat Biol 11:7–26

    Article  Google Scholar 

  • Iseri OD, Korpe DA, Yurtcu E, Sahin F, Haberal M (2011) Copper-induced oxidative damage, antioxidant response and genotoxicity in Lycopersicum esculentum Mill. and Cucumis sativus L. Plant Cell Rep 30:1713–1721

    Article  CAS  Google Scholar 

  • Janaki Devi V, Nagarani N, YokeshBabu M, Vijayalakshimi N, Kumaraguru AK (2012) Genotoxic effects of profenofos on the marine fish, Therapon jarbua. Toxicol Mech Method 22:111–117

    Article  CAS  Google Scholar 

  • Jin X, Yang X, Islam E, Liu D, Mahmood Q (2008) Effect of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. J Hazard Mater 156:387–397

    Article  CAS  Google Scholar 

  • Johnson HL, Stauber JL, Adams MS, Jolley DF (2007) Copper and zinc tolerance of two tropical microalgae after copper acclimation. Environ Toxicol 22:234–244

    Article  CAS  Google Scholar 

  • Kumar M, Anisha PA, Kumari P, Reddy CRK, Gupta V, Jha B (2010) Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals 23:315–325

    Article  CAS  Google Scholar 

  • Kumar M, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2012) Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiol Biochem 51:129–138

    Article  CAS  Google Scholar 

  • Lane TW, Morel FMM (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol 123:345–352

    Article  CAS  Google Scholar 

  • Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Env Sci Technol 39:1921–1931

    Article  CAS  Google Scholar 

  • Luoma SN, Rainbow PS (2008) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Env Sci Technol 39:1921–1931

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35:524–533

    Article  CAS  Google Scholar 

  • Mehta R, Templeton DM, O’Brien PJ (2006) Mitochondrial involvement in genetically determined transition metal toxicity. II. Copper toxicity. Chem Biol Interact 163:77–85

    Article  CAS  Google Scholar 

  • Mendes LF, Villela LZ, Colepicolo P, Soriano EM, Stevani CV, Yokoya NS (2013) Metal cation toxicity in the alga Gracilaria domingensis as evaluated by the daily growth rates in synthetic seawater. J Appl Phycol 25:1939–1947

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Murthy SBK, Umamaheswara Roa M (2003) Effects of industrial wastes on the growth and reproductive stages of macroalgae of Visakhapatnam coastline, east coast of India. Indian J Mar Sci 32:57–66

    Google Scholar 

  • Nagarani N, JanakiDevi V, YokeshBabu M, Kumaraguru AK (2012) Protective effect of Kappaphycus alvarezii (Rhodophyta) extract against DNA damage induced by mercury chloride in marine fish. Toxicol Environ Chem 94:1401–1410

    Article  CAS  Google Scholar 

  • Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301

    Article  CAS  Google Scholar 

  • Páez-Osuna F, Ochoa-Izaguirre MJ, Bojórquez-Leyva H, MichelReynoso IL (2000) Macroalgae as biomonitors of heavy metal availability in coastal lagoons from the subtropical Pacific of Mexico. Bull Environ Contam Toxicol 64:846–851

    Article  Google Scholar 

  • Palanikumar L, Rajee M, Kumaraguru AK (2011) Role of epibiotic algae on the recruitment and biomass of horse mussels, Modiolus spp. in Pudhumadam Coast, Gulf of Mannar. World J Zool 6:173–178

    Google Scholar 

  • Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2012a) Biochemical response of anthracene and benzo [a] pyrene in milkfish Chanos chanos. Ecotoxicol Environ Saf 75:187–197

    Article  CAS  Google Scholar 

  • Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2012b) Genotoxic assessment of anthracene and benzo [a] pyrene to milkfish Chanos chanos. Toxicol Environ Chem 94:350–363

    Article  CAS  Google Scholar 

  • Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2013a) Toxicity, biochemical and clastogenic response of chlorpyrifos and carbendazime in milkfish Chanos chanos. Int J Environ Sci Technol. doi:10.1007/s13762-013-0264-6

    Google Scholar 

  • Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2013b) Toxicity, feeding rate and growth rate response to sub-lethal concentrations of anthracene and benzo [a] pyrene in milkfish Chanos chanos (Forskkal). Bull Environ Contam Toxicol 90:60–68

    Article  CAS  Google Scholar 

  • Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018

    Article  CAS  Google Scholar 

  • Prasad N (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:535–545

    Article  Google Scholar 

  • Rainbow PS (2005) Biomonitoring of trace metals in estuarine and marine environments. Australas J Ecotoxicol 12:107–122

    Google Scholar 

  • Reddy MK, Alexander-Lindo RL, Nair MG (2005) Relative inhibition of lipid peroxidation, cyclooxygenase enzymes and human tumor cell proliferation by natural food colors. J Agric Food Chem 53:9268–9273

    Article  CAS  Google Scholar 

  • Rodríguez Meza D (2005) Caracterización geoquímica por components mayores y elementos traza de sedimentos de los ambientes marinos costeros adyacentes a la península de Baja California. Ph.D. Dissertation, Centro Interdisciplinario de Ciencias Marinas-Instituto Politécnico Nacional, La Paz, Mexico (in Spanish)

  • Rodríguez-Figueroa GM, Shumilin E, Sánchez-Rodríguez I (2009) Heavy metal pollution monitoring using the brown seaweed Padina durvillaei in the coastal zone of the Santa Rosalía mining region, Baja California Peninsula, Mexico. J Appl Phycol 21:19–26

    Article  Google Scholar 

  • Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 1973(179):588–590

    Article  Google Scholar 

  • Saez CA, Lobos MG, Macaya EC, Oliva D, Quiroz W, Brown MT (2012) Variation in patterns of metal accumulation in thallus Parts of Lessonia trabeculata (Laminariales; Phaeophyceae): implications for biomonitoring. PLos One 7:e50170–e50180

    Article  CAS  Google Scholar 

  • Simon DF, Davis TA, Tercier-Waeber ML, England R, Wilkinson KJ (2011) In situ evaluation of cadmium biomarkers in green algae. Environ Pollut 159:2630–2636

    Article  CAS  Google Scholar 

  • Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246

    Article  CAS  Google Scholar 

  • Sinha A (1972) Catalase—an extra ordinary enzyme. Science 210:71–82

    Google Scholar 

  • Sprague JB (1973) The ABCs of pollutant bioassay using fish. In: Cairns J, Dickson DL (eds) Biological methods for assessment of water quality, vol 528. American Society for Testing and Materials, Philadelphia, pp 6–30

    Chapter  Google Scholar 

  • Stauber JL, Andrade S, Ramirez M, Adams M, Correa JA (2005) Copper bioavailability in a coastal environment of Northern Chile: comparison of bioassay and analytical speciation approaches. Mar Pollut Bull 50:1363–1372

    Article  CAS  Google Scholar 

  • Stengel DB, McGrath H, Morrison LJ (2005) Tissue Cu, Fe and Mn concentrations in different-aged and different functional thallus regions of three brown algae from western Ireland. Estuar Coast Shelf Sci 65:687–696

    Article  CAS  Google Scholar 

  • Tsuji N, Nishikori S, Iwabe O, Matsumoto S, Shiraki K, Miyasaka H, Takagi M, Miyamoto K, Hirata K (2005) Comparative analysis of the two-step reaction catalyzed by prokaryotic and eukaryotic phytochelatin synthase by an ion-pair liquid chromatography assay. Planta 222:181–191

    Article  CAS  Google Scholar 

  • United States Environmental Protection Agency (USEPA) (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. 5th ed. (October). Washington, DC: United States Environmental Protection Agency, Office of Water (4303T). EPA-821-R-02-012, pp 275

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    Article  CAS  Google Scholar 

  • Wang W, Lampi MA, Huang XD, Gerhardt K, Dixon DG, Greenberg BM (2008) Assessment of mixture toxicity of copper, cadmium, and phenanthrenequinone to the marine bacterium Vibrio fischeri. Environ Toxicol 166–177

  • Wang D, Lermusiaux PFJ, Haley PJ, Eickstedt D, Leslie WG, Schmidt H (2009) Acoustically focused adaptive sampling and on-board routing for marine rapid environmental assessment. J Mar Syst 78:S393–S407

    Article  Google Scholar 

  • Wells PG, Depledge MH, Butler JN, Manock JJ, Knap AH (2001) Rapid toxicity assessment and biomonitoring of marine contaminants exploiting the potential of rapid biomarker assays and microscale toxicity tests. Mar Pollut Bull 42:799–804

    Article  CAS  Google Scholar 

  • Wu TM, Lee TM (2008) Regulation of activity and gene expression of antioxidant enzymes in Ulva fasciata Delile (Ulvales, Chlorophyta) in response to excess copper. Phycologia 47:346–360

    Article  CAS  Google Scholar 

  • Yan K, Chen W, He X, Zhang G, Xu S, Wang L (2010) Responses of photosynthesis, lipid peroxidation and antioxidant system in leaves of Quercus mongolica to elevated O3. Environ Exp Bot 69:198–204

    Article  CAS  Google Scholar 

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  1. L. Palanikumar

    Present address: Anna University, Chennai, 600025, India

Authors and Affiliations

  1. Department of Marine and Coastal Studies, School of Energy, Environment and Natural Resources, Madurai Kamaraj University, Madurai, 625021, Tamilnadu, India

    M. Yokesh Babu, L. Palanikumar, N. Nagarani, V. Janaki Devi, S. Ramesh Kumar, C. M. Ramakritinan & A. K. Kumaraguru

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  1. M. Yokesh Babu
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  2. L. Palanikumar
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  3. N. Nagarani
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Babu, M.Y., Palanikumar, L., Nagarani, N. et al. Cadmium and copper toxicity in three marine macroalgae: evaluation of the biochemical responses and DNA damage. Environ Sci Pollut Res 21, 9604–9616 (2014). https://doi.org/10.1007/s11356-014-2999-0

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