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Bioaccumulation of PBDE congener 2,2′,4,4′-tetrabromodiphenyl ether by Heterosigma akashiwo in response to different nutrient concentrations

  • Original research paper
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Oceanological and Hydrobiological Studies

Abstract

Changes in the bioaccumulation of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) in the marine alga Heterosigma akashiwo (Raphidophyceae) were examined for different concentrations of nitrate (0, 128, and 512 μmol dm−3) and phosphate (0, 8, and 32 μmol dm−3) in the semi-continuous culture with 20% renewal rate. The BDE-47 content per cell and per culture, as well as the accumulated percentage of available BDE-47, presented a significant decreasing trend with the increase in nitrate and phosphate concentrations. The N-0 (4.0 × 10−6 ng cell−1) and P-0 (5.8 × 10−6 ng cell−1) treatments had significantly higher BDE-47 content per cell than other treatments. In comparison, the difference in BDE-47 per algal culture and accumulated percentage between the nitrate treatments or phosphate treatments was not as obvious as the BDE-47 content per cell. BDE-47 per cell presented significantly negative correlation with nitrate and phosphate concentrations, and the accumulated BDE-47 was in positive correlation with lipid content. log BAFlip for BDE-47 in H. akashiwo ranged from 6.70 to 7.25. The results of this study indicate that variation in BDE-47 accumulation by H. akashiwo corresponds to the change in cellular lipid content induced by different nitrate and phosphate concentrations.

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References

  • Berdalet, E., Latasa, M. & Estrada, M. (1994). Effects of nitrogen and phosphorus starvation on nucleic acid and protein content of Heterocapsa sp. Journal of Plankton Research, 16(4), 303–316.

    Article  Google Scholar 

  • Berglund, O., Larsson, P., Ewald, G. & Okla, L. (2000). Bioaccumulation and differential partitioning of polychlorinated biphenyls in freshwater, planktonic food webs. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1160–1168.

    Article  Google Scholar 

  • Bligh, E.G. & Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37, 911–917.

    Article  Google Scholar 

  • Borghesi, N., Corsolini, S., & Focardi, S. (2008). Levels of polybrominated diphenyl ethers (PBDEs) and organochlorine pollutants in two species of Antarctic fish (Chionodraco hamatus and Trematomus bernacchii). Chemosphere, 73(2), 155–160.

    Article  Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. Analytical Biochemistry, 72, 248–254.

    Article  Google Scholar 

  • Carlson, D.L. & Swackhamer, D.L. (2006). Results from the US Great Lakes fish monitoring program and effects of lake processes on bioaccumulative contaminant concentrations. Journal of Great Lakes Research, 32, 370–385.

    Article  Google Scholar 

  • Chiuchiolo, A.L., Dickhut, R.M., Cochran, M.A. & Ducklow, H.W. (2004). Persistent organic pollutants at the base of the Antarctic marine food Web. Environmental Science and Technology, 38(13), 3551–3557.

    Article  Google Scholar 

  • Cunningham, S.D. & Berti, W.R. (1993). Remediation of contaminated soils with green plants: an overview. In Vitro Cellular & Developmental Biology, 29(4), 207–212.

    Article  Google Scholar 

  • Datta, S. (2001). Relationship between PCB uptake and nutrient limitation in three algal species. Unpublished doctoral dissertation, Drexel University, Philadelphia, PA, USA.

    Google Scholar 

  • De Wit, C.A. (2002). An overview of brominated flame retardants in the environment. Chemosphere, 46(5), 583–624.

    Article  Google Scholar 

  • De Wit, C.A., Alaee, M. & Muir, D.C.G. (2006) Levels and trends of brominated flame retardants in the Arctic. Chemosphere, 64(2), 209–233.

    Article  Google Scholar 

  • Fang K. (2006). Studies on the adsorption of PCBs to marine microalgae. Unpublished Master Thesis, Dalian Maritime University, Dalian, China (in Chinese with English abstract).

    Google Scholar 

  • Fogg, G.E. (1959). Nitrogen nutrition and metabolic patterns in algae. Symposia of the Society for Experimental Biology, 13, 106–125.

    Google Scholar 

  • Fontana, A.R., Silva, M.F., Martinez, L.D., Wuilloud R.G. & Altamirano, J.C. (2009). Determination of polybrominated diphenyl ethers in water and soil samples by cloud point extraction-ultrasound-assisted back-extraction-gas chromatography-mass spectrometry. Journal of Chromatography A, 1216,4339–4346.

    Article  Google Scholar 

  • Gerofke, A., Komp, P. & McLachlan, M.S. (2005). Bioconcentration of persistent organic pollutants in four species of marine phytoplankton. Environmental Toxicology and Chemistry, 24, 2908–2917.

    Article  Google Scholar 

  • Grasshoff, K. (1976). Methods of Seawater Analysis. Verlag Chemie, Weinheim New York.

    Google Scholar 

  • Guan, Y.F., Samuel Sojinu, O.S., Li S.M. & Zeng, E.Y. (2009). Fate of polybrominated diphenyl ethers in the environment of the Pearl River Estuary, South China. Environmental Pollution, 157, 2166–2172.

    Article  Google Scholar 

  • Guan, Y.F., Tu, X.Y. & Wu H.H. (2011). Distribution and source of polybrominated diphenyl ethers (PBDEs). Ecology and Environmental Sciences, 20(3), 474–479(in Chinese with English abstract).

    Google Scholar 

  • Guo, J.Y., Wu, F.C., Mai, B.X., Luo, X.J. & Zeng, E.Y. (2007). Polybrominated diphenyl ethers in seafood products of South China. Journal of Agricultural and Food Chemistry, 55, 9152–9158.

    Article  Google Scholar 

  • Hale, R.C., Alaeeb, M.J., Manchester-Neesvigc, B., Stapletond, H.M. & Ikonomou, M.G. (2003). Polybrominated diphenyl ether flame retardants in the North American environment. Environment International, 29(6), 771–779.

    Article  Google Scholar 

  • Halling-Sørensen, B., Nyholm, N., Kusk, K.O. & Jacobsson, E. (2000). Influence of nitrogen status on the bioconcentration of hydrophobic organic compounds to Selenastrum capricornutum. Ecotoxicology and Environmental Safety, 45, 33–42.

    Article  Google Scholar 

  • Hites, R.A. (2004). Polybrominated diphenylethers in the environment and in people: a meta-analysis of concerntrations. Environmental Science and Technology, 38, 945–956.

    Article  Google Scholar 

  • Huang, X.P., Huang, L.M. & Yue. W.Z. (2003). The characteristics of nutrients and eutrophication in the Pearl River estuary, South China. Marine Pollution Bulletin, 47(1–6), 30–36.

    Article  Google Scholar 

  • Ji, D.W., Yang J.Q., Gao Z.H. & Jia Y.G. (2007). Eutrophication assessment of the western sea area in the Laizhou Bay during the low water period. Journal of Marine Science Bulletin, 26(1), 78–81(in Chinese with English abstract).

    Google Scholar 

  • Jin, J., Liu, W.Z., Wang, Y. & Tang. X.Y. (2008). Levels and distribution of polybrominated diphenyl ethers in plant, shellfish and sediment samples from Laizhou Bay in China. Chemosphere, 71(6), 1043–1050.

    Article  Google Scholar 

  • Justic, D., Rabalais, N.N., Turner, R.E. & Dortch, Q. (1995). Changes in nutrient structure of river-dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuarine Coastal and Shelf Science, 40, 339–356.

    Article  Google Scholar 

  • Khan, S., Arakawa, O. & Onoue, Y. (1997). Neurotoxins in a toxic red tide of Heterosigma akashiwo (Raphidophyceae) in Kagoshima Bay, Japan. Aquaculture Research, 28(1), 9–14.

    Article  Google Scholar 

  • Khozin-Goldberg, I. & Cohen, Z. (2006). The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry, 67, 696–701.

    Article  Google Scholar 

  • Kilham, S.S. (1998). Effects of physiological state on the bioaccumulation of toxic chemicals in algae and their transfer to zooplankton. Verhandlungen-Internationale Vereinigung für theoretische und angewandte Limnologie, 26, 1734–1736.

    Google Scholar 

  • Kilham, S.S., Kreeger, D.A., Goulden, C.E. & Lynn, S.G. (1997). Effects of nutrient limitation on biochemical constituents of Ankystrodesmus falcatus. Freshwater Biology, 38, 591–596.

    Article  Google Scholar 

  • Kochert, G. (1978). Carbohydrate determination by phenol-sulfuric acid method. In: J.A. Hellebust & J.S. Craige (Eds.), Handbook of physiological and biochemical method s (pp.95–97). Cambridge University Press, London.

    Google Scholar 

  • Lai, J.X., Yu, Z.M., Song, X.X., Cao, X.H. & Han. X.T. (2011). Responses of the growth and biochemical composition of Prorocentrum donghaiense to different nitrogen and phosphorus concentrations. Journal of Experimental Marine Biology and Ecology, 405, 6–17.

    Article  Google Scholar 

  • Landry, M.R. & Hassett, R.P. (1982). Estimating the grazing impact of marine microzooplankton. Marine Biology, 67, 283–288.

    Article  Google Scholar 

  • Law, R.J., Allchin, C.R., de Boer, J., Covaci, A., Herzke, D., Lepom, P., Morris, S., Tronczynski J. & De Wit, C.A. (2006). Levels and trends of brominated flame retardants in the European environment. Chemosphere, 64(2), 187–208.

    Article  Google Scholar 

  • Li, M., Gong, R., Rao, X., Liu, Z.H. & Wang, X. (2005). Effects of nitrate concentration on growth and fatty acid composition of the marine microalgae Pavlova viridis (Prymnesiophyceae). Annals of Microbiology, 55, 51–55.

    Google Scholar 

  • Liu, S.M., Zhang, J., Chen, H.T. & Zhang, G.S. (2005). Factors influencing nutrient dynamics in the eutrophic Jiaozhou Bay, North China. Progress in Oceanography, 66(1), 66–85.

    Article  Google Scholar 

  • Lourenço, S.O., Marquez, U.M.L., Mancinifilho, J., Barbarino, E. & Aidar, E. (1997). Changes in biochemical profile of Tetraselmis gracilis I. Comparison of two culture media. Aquaculture, 148, 153–168.

    Google Scholar 

  • Luo, X.J., Yu, M., Mai, B.X. & Chen, S.J. (2008). Distribution and partition of polybrominated diphenyl ethers (PBDEs) in water of the Zhujiang River Estuary. Chinese Science Bulletin, 53(4), 493–500.

    Article  Google Scholar 

  • Lynn, S.G., Price, D.J., Birge, W.J. & Kilham, S.S. (2007). Effect of nutrient availability on the uptake of PCB congener 2,2′,6,6′-tetrachlorobiphenyl by a diatom (Stephanodiscus minutulus) and transfer to a zooplankton (Daphnia pulicaria). Aquatic Toxicology, 83, 24–32.

    Article  Google Scholar 

  • Meng, X.Z., Yu, L.P., Guo, Y., Mai, B.X. & Zeng, E.Y. (2008). Congener-specific distribution of polybrominated diohenyl ethers in fish of China: implication for input sources. Environmental Toxicology and Chemistry, 27, 67–72.

    Article  Google Scholar 

  • Merzlyak, M.N., Chivkunova, O.B., Gorelova, O.A., Reshetnikova, I.V., Solovchenko, A.E., Khozin-Goldberg, I. & Cohen, Z. (2007). Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incise (Trebouxiophyceae, Chlorophyta). Journal of Applied Phycology, 43, 833–843.

    Article  Google Scholar 

  • Ohta, S., Ishizuka, D., Nishimura, H., Nakao, T., Aozasa, O., Shimidzu, Y., Ochiai, F., Kida, T., Nishi, M. & Miyata, H. (2002). Comparison of polybrominated diphenyl ethers in fish, vegetables, and meats and levels in human milk of nursing women in Japan. Chemosphere, 46(5), 689–696.

    Article  Google Scholar 

  • Oros, D.R., Hoover, D., Rodigari, F., Crane, D. & Sericano, J. (2005). Levels and distribution of polybrominated diphenyl ethers in water, surface sediments, and bivalves from the San Francisco Estuary. Environmental Science and Technology, 39(1), 33–41.

    Article  Google Scholar 

  • Pande, S.V., Parvin, R. & Venkitasubramanian, T.A. (1963). Microdetermination of lipids and serum total fatty acids. Analytical Biochemistry, 6, 415–425.

    Article  Google Scholar 

  • Rahman, F., Langford, K.H., Scrimshaw, M.D. & Lester, J. N. (2001). Polybrominated diphenyl ether (PBDE) flame retardants. Science of the Total Environment, 275(1–3), 1–17.

    Article  Google Scholar 

  • Rausch, T. (1981). The estimation of micro-algal protein content and its meaning to the evaluation of algal biomass I. Comparison of methods for extracting protein. Hydrobiologia, 78, 237–251.

    Article  Google Scholar 

  • Sellström, U., Jansson, B., Kierkegaard, A., de Wit, C., Odsjö, T. & Olsson, M. (1993). Polybrominated diphenyl ethers (PBDE) in biological samples from the Swedish environment. Chemosphere, 26(9), 1703–1718.

    Article  Google Scholar 

  • Smith, V.H. (2003). Eutrophication of freshwater and coastal marine ecosystems: a global problem. Environmental Science and Pollution Research, 10(2), 126–139.

    Article  Google Scholar 

  • Stange, K. & Swackhamer, D.L. (1994). Factors affecting phytoplankton species-specific differences in accumulation of 40 polychlorinated biphenyls (PCBs). Environmental Toxicology and Chemistry, 13, 1849–1860.

    Article  Google Scholar 

  • Strickland, J.D.H. & Parsons, T.R. (1972). A practical handbook of seawater analysis. Fisheries Research Board of Canada, 167, 311.

    Google Scholar 

  • Suzuki, G., Nose, K., Takigami, H., Takahashi, S. Sakai, S.I. (2006). PBDEs and PBDD/Fs in house and office dust from Japan. Organohalogen Compounds, 68, 1843–1846.

    Google Scholar 

  • Swackhamer, D.L. (1985). The Role of water particle partitioning and sedimentation in controlling the fate and transport of PCBs in lakes. Unpublished doctoral dissertation, University of Wisconsin, Madison, WI, USA.

    Google Scholar 

  • Swackhamer, D.L. & Skoglund, R.S. (1993). Bioaccumulation of PCBs by algae: kinetics versus equilibrium. Environmental Toxicology and Chemistry, 12, 831–838.

    Article  Google Scholar 

  • Thompson, G.A. Jr. (1996). Lipids and membrane function in green algae. Biochimica et Biophysica Acta, 1302, 17–45.

    Article  Google Scholar 

  • Wang, Y.W., Jiang, G.B., Lam P.K.S. & Li, A. (2007). Polybrominated diphenyl ether in the East Asian environment: A critical review. Environment International, 33(7), 963–973.

    Article  Google Scholar 

  • Yang Y.L., Pan, J., Li, Y., Yin, X.C. & Hi, L. (2004). Persistent organic pollutants PCNs and PBDEs in sediments from coastal waters of Qingdao, Shandong Peninsula. Chinese Science Bulletin, 49(1), 98–106.

    Google Scholar 

  • Zhao, Y.F., Yu, Z.M., Song, X.X. & Cao, X.H. (2009). Biochemical compositions of two dominant bloom-forming species isolated from the Yangtze River Estuary in response to different nutrient conditions. Journal of Experimental Marine Biology and Ecology, 368(1), 30–36.

    Article  Google Scholar 

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Correspondence to Chao Chai.

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Ge, W., Yin, X., Chai, C. et al. Bioaccumulation of PBDE congener 2,2′,4,4′-tetrabromodiphenyl ether by Heterosigma akashiwo in response to different nutrient concentrations. Ocean and Hydro 42, 139–148 (2013). https://doi.org/10.2478/s13545-013-0067-x

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