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Induced production of brominated aromatic compounds in the alga Ceramium tenuicorne

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Abstract

In the Baltic Sea, high concentrations of toxic brominated aromatic compounds have been detected in all compartments of the marine food web. A growing body of evidence points towards filamentous algae as a natural producer of these chemicals. However, little is known about the effects of environmental factors and life history on algal production of brominated compounds. In this study, several congeners of methoxylated polybrominated diphenyl ethers (MeO-PBDEs), hydroxylated polybrominated diphenyl ethers (OH-PBDEs) and brominated phenols (BPs) were identified in a naturally growing filamentous red algal species (Ceramium tenuicorne) in the Baltic Sea. The identified substances displayed large seasonal variations in the alga with a concentration peak in July. Production of MeO-/OH-PBDEs and BPs by C. tenuicorne was also established in isolated clonal material grown in a controlled laboratory setting. Based on three replicates, herbivory, as well as elevated levels of light and salinity in the culture medium, significantly increased the production of 2,4,6-tribromophenol (2,4,6-TBP). Investigation of differences in production between the isomorphic female, male and diploid clonal life stages of the alga grown in the laboratory revealed a significantly higher production of 2,4,6-TBP in the brackish water female gametophytes, compared to the corresponding marine gametophytes. Even higher concentrations of 2,4,6-TBP were produced by marine male gametophytes and sporophytes.

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References

  • Abrahamsson K, Choo KS, Pedersen M, Johansson G, Snoeijs P (2003) Effects of temperature on the production of hydrogen peroxide and volatile halocarbons by brackish-water algae. Phytochemistry 64:725–734

    Article  CAS  Google Scholar 

  • Arnoldsson K, Andersson PL, Haglund P (2012) Photochemical formation of polybrominated dibenzo-p-dioxins from environmentally abundant hydroxylated polybrominated diphenyl ethers. Environ Sci Technol 46:7567–7574

    Article  CAS  Google Scholar 

  • Canton R, Sanderson J, Letcher R, Bergman Å, Van den Berg M (2005) Inhibition and induction of aromatase (CYP19) activity by brominated flame retardants in H295R human adrenocortical carcinoma cells. Toxicol Sci 88:447–455

    Article  CAS  Google Scholar 

  • Chung HY, Ma WCJ, Ang PO, Kim JS, Chen F (2003) Seasonal variations of bromophenols in brown algae (Padina arborescens, Sargassum siliquastrum and Lobophora variegata) collected in Hong Kong. J Agric Food Chem 51:2619–2624

    Article  CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Dring M (2005) Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv Bot Res 43:176–207

    Google Scholar 

  • Eklund B (2005) Development of a growth inhibition test with the marine and brackish water red alga Ceramium tenuicorne. Mar Pollut Bull 50:921–930

    Article  CAS  Google Scholar 

  • Flodin C, Helidoniotis F, Whitfield F (1998) Seasonal variation in bromophenol content and bromoperoxidase activity in Ulva lactuca. Phytochemistry 51:135–138

    Article  Google Scholar 

  • Fox J (2005) The R commander: a basic statistics graphical user interface to R. J Stat Softw 14:1–42

    Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339

    Article  Google Scholar 

  • Haglund P, Zook D, Buser HR, Hu J (1997) Identification and quantification of polybrominated diphenyl ethers and methoxy-polybrominated diphenyl ethers in Baltic biota. Environ Sci Technol 31:3281–3287

    Article  CAS  Google Scholar 

  • Hakk H, Letcher RJ (2003) Metabolism in the toxicokinetics and fate of brominated flame retardants—a review. Environ Int 29:801–828

    Article  CAS  Google Scholar 

  • Haldén A, Nyholm J, Andersson P, Holbech H, Norrgren L (2010) Oral exposure of adult zebrafish (Danio rerio) to 2,4,6-tribromophenol affects reproduction. Aquat Toxicol 100:30–37

    Article  Google Scholar 

  • Hovander L, Athanasiadou M, Asplund L, Jensen S, Klasson-Wehler E (2000) Extraction and cleanup methods for analysis of phenolic and neutral organohalogens in plasma. J Anal Toxicol 24:696–703

    Article  CAS  Google Scholar 

  • Jensen S, Häggberg L, Jörundsdottir H, Odham G (2003) A quantitative lipid extraction method for residue analysis of fish involving nonhalogenated solvents. J Agric Food Chem 51:5607–5611

    Article  CAS  Google Scholar 

  • Jensen S, Lindqvist D, Asplund L (2009) Lipid extraction and determination of halogenated phenols and alkylphenols as their pentafluorobenzoyl derivatives in marine organisms. J Agric Food Chem 57:5872–5877

    Article  CAS  Google Scholar 

  • Kammann U, Vobach M, Wosniok W (2006) Toxic effects of brominated indoles and phenols on zebrafish embryos. Arch Environ Contam 51:97–102

    Article  CAS  Google Scholar 

  • Legler J (2008) New insights into the endocrine disrupting effects of brominated flame retardants. Chemosphere 73:216–222

    Article  CAS  Google Scholar 

  • Legradi J, Dahlberg AK, Cenijn P, Marsh G, Asplund L, Bergman A, Legler J (2014) Disruption of oxidative phosphorylation (OXPHOS) by hydroxylated polybrominated diphenyl ethers (OH-PBDEs). Marine Environment. Environ Sci Technol 48:1703–1711

    Article  Google Scholar 

  • Li JY, Agatsuma Y, Taniguchi K (2009) Inhibitory effect of 2,4-dibromophenol and 2,4,6-tribromophenol on settlement and survival of larvae of the Japanese Abalone Haliotis discus hannai ino. J Shellfish Res 28:877–882

    Article  Google Scholar 

  • Löfstrand K, Malmvärn A, Haglund P, Bignert A, Bergman Å, Asplund L (2010) Brominated phenols, anisoles, and dioxins present in blue mussels from the Swedish coastline. Environ Sci Pollut Res 17:1460–1468

    Article  Google Scholar 

  • Löfstrand K, Liu X, Lindqvist D, Jensen S, Asplund L (2011) Seasonal variation of hydroxylated and methoxylated brominated diphenyl ethers in blue mussels from the Baltic Sea. Chemosphere 84:527–532

    Article  Google Scholar 

  • Malmvärn A, Marsh G, Kautsky L, Athanasiadou M, Bergman Å, Asplund L (2005) Hydroxylated and methoxylated brominated diphenyl ethers in the red algae Ceramium tenuicorne and blue mussels from the Baltic Sea. Environ Sci Technol 39:2990–2997

    Article  Google Scholar 

  • Malmvärn A, Zebühr Y, Kautsky L, Bergman Å, Asplund L (2008) Hydroxylated and methoxylated polybrominated diphenyl ethers and polybrominated dibenzo-p-dioxins in red alga and cyanobacteria living in the Baltic Sea. Chemosphere 72:910–916

    Article  Google Scholar 

  • Marsh G, Athanasiadou M, Athanassiadis I, Sandolm A (2006) Identification of hydroxylated metabolites in 2,2′,4,4′-tetrabromodiphenyl ether exposed rats. Chemosphere 63:690–697

    Article  CAS  Google Scholar 

  • Matlock D, Ginsburg D, Paul V (1999) Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia 399:267–273

    Google Scholar 

  • Meerts IATM, van Zanden JJ, Luijks EAC, van Leewen-Bol I, Marsh G, Jakobsson E, Bergman Å, Brouwer A (2000) Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicol Sci 56:95–104

    Article  CAS  Google Scholar 

  • Meerts I, Letcher R, Hoving S, Marsh G, Bergman Å, Lemmen J, van der Burg B, Brouwer A (2001) In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PBDEs, and polybrominated bisphenol A compounds. Environ Heal Perspect 109:399–407

    Article  CAS  Google Scholar 

  • Olsen C, Meussen-Elholm E, Holme J, Hongslo J (2001) Brominated phenols: characterization of estrogen-like activity in the human breast cancer cell-line MCF-7. Toxicol Lett 129:55–63

    Article  Google Scholar 

  • Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169

    Article  CAS  Google Scholar 

  • Paul VJ, Fenical W (1987) Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. In: Scheuer PJ (ed) Bioorganic marine chemistry. Vol. I. Springer-Verlag, Berlin, pp 1–37

    Chapter  Google Scholar 

  • Pedersén M, Collen J, Abrahamsson K, Ekdahl A (1996) Production of halocarbons from seaweeds: an oxidative stress reaction? Sci Mar 60:257–263

    Google Scholar 

  • Pereira R, Soares A, Teixeira V, Villaca R, Da Gama B (2004) Variation in chemical defenses against herbivory in southwestern Atlantic Stypopodium zonale (Phaeophyta). Bot Mar 47:202–208

    Article  Google Scholar 

  • Puglisi M, Paul V (1997) Intraspecific variation in the red alga Portieria hornemannii: monoterpene concentrations are not influenced by nitrogen or phosphorus enrichment. Mar Biol 128:161–170

    Article  CAS  Google Scholar 

  • Shibata T, Hama Y, Miyasaki T, Ito M, Nakamura T (2006) Extracellular secretion of phenolic substances from living brown algae. J Appl Phycol 18:787–794

    Article  CAS  Google Scholar 

  • Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defenses or valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612–618

    Article  Google Scholar 

  • Tuomi J (1992) Toward integration of plant defence theories. Trends Ecol Evol 7:365–367

    Article  CAS  Google Scholar 

  • Ucan-Marin F, Arukwe A, Mortensen A, Gabrielsen GW, Fox GA, Letcher RJ (2009) Recombinant transthyretin purification and competitive binding with organohalogen compounds in two gull species (Larus argentatus and Larus hyperboreus). Toxicol Sci 107:440–450

    Article  CAS  Google Scholar 

  • Van Boxtel A, Kamstra J, Cenjin P, Pieteerse B, Wagner M, Antink M, Krab K, Vaan der Burg B, Marsch G, Legler J (2008) Microarray analysis reveals a mechanism of phenolic polybrominated diphenyl ether toxicity in zebrafish. Environ Sci Technol 42:1773–1779

    Article  Google Scholar 

Download references

Acknowledgments

We thank Henrik Dahlgren at the Museum of Natural History in Stockholm for collecting the alga from Nämdö Island. The research was funded by the Swedish Environmental Protection Agency and the Marine Environment Research Funds, through the Baltic Ecosystem Adaptive Management (BEAM).

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Authors and Affiliations

  1. Department of Environmental Science and Analytical Chemistry, Stockholm University, Stockholm, Sweden

    Elin Dahlgren, Dennis Lindqvist, Britta Eklund & Lillemor Asplund

  2. AquaBiota Water Research, 115 50, Stockholm, Sweden

    Carolina Enhus

Authors
  1. Elin Dahlgren
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  2. Carolina Enhus
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  3. Dennis Lindqvist
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  4. Britta Eklund
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  5. Lillemor Asplund
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Correspondence to Elin Dahlgren or Lillemor Asplund.

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Dahlgren, E., Enhus, C., Lindqvist, D. et al. Induced production of brominated aromatic compounds in the alga Ceramium tenuicorne . Environ Sci Pollut Res 22, 18107–18114 (2015). https://doi.org/10.1007/s11356-015-4907-7

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  • DOI: https://doi.org/10.1007/s11356-015-4907-7

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