Environmental Science and Pollution Research

, Volume 22, Issue 22, pp 18107–18114 | Cite as

Induced production of brominated aromatic compounds in the alga Ceramium tenuicorne

  • Elin DahlgrenEmail author
  • Carolina Enhus
  • Dennis Lindqvist
  • Britta Eklund
  • Lillemor AsplundEmail author
Research Article


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.


Secondary metabolites Natural production Chemical pollutant Bromophenols Seasonal variations Stress-induced production 



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).

Supplementary material

11356_2015_4907_MOESM1_ESM.docx (129 kb)
ESM 1 (DOCX 128 kb)


  1. 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 64:725–734CrossRefGoogle Scholar
  2. Arnoldsson K, Andersson PL, Haglund P (2012) Photochemical formation of polybrominated dibenzo-p-dioxins from environmentally abundant hydroxylated polybrominated diphenyl ethers. Environ Sci Technol 46:7567–7574CrossRefGoogle Scholar
  3. 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 88:447–455CrossRefGoogle Scholar
  4. 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 51:2619–2624CrossRefGoogle Scholar
  5. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  6. Dring M (2005) Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv Bot Res 43:176–207Google Scholar
  7. Eklund B (2005) Development of a growth inhibition test with the marine and brackish water red alga Ceramium tenuicorne. Mar Pollut Bull 50:921–930CrossRefGoogle Scholar
  8. Flodin C, Helidoniotis F, Whitfield F (1998) Seasonal variation in bromophenol content and bromoperoxidase activity in Ulva lactuca. Phytochemistry 51:135–138CrossRefGoogle Scholar
  9. Fox J (2005) The R commander: a basic statistics graphical user interface to R. J Stat Softw 14:1–42Google Scholar
  10. Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339CrossRefGoogle Scholar
  11. 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 31:3281–3287CrossRefGoogle Scholar
  12. Hakk H, Letcher RJ (2003) Metabolism in the toxicokinetics and fate of brominated flame retardants—a review. Environ Int 29:801–828CrossRefGoogle Scholar
  13. 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 100:30–37CrossRefGoogle Scholar
  14. 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 24:696–703CrossRefGoogle Scholar
  15. 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 51:5607–5611CrossRefGoogle Scholar
  16. 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 57:5872–5877CrossRefGoogle Scholar
  17. Kammann U, Vobach M, Wosniok W (2006) Toxic effects of brominated indoles and phenols on zebrafish embryos. Arch Environ Contam 51:97–102CrossRefGoogle Scholar
  18. Legler J (2008) New insights into the endocrine disrupting effects of brominated flame retardants. Chemosphere 73:216–222CrossRefGoogle Scholar
  19. 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 48:1703–1711CrossRefGoogle Scholar
  20. 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 28:877–882CrossRefGoogle Scholar
  21. 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 17:1460–1468CrossRefGoogle Scholar
  22. 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 84:527–532CrossRefGoogle Scholar
  23. 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 39:2990–2997CrossRefGoogle Scholar
  24. 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 72:910–916CrossRefGoogle Scholar
  25. Marsh G, Athanasiadou M, Athanassiadis I, Sandolm A (2006) Identification of hydroxylated metabolites in 2,2′,4,4′-tetrabromodiphenyl ether exposed rats. Chemosphere 63:690–697CrossRefGoogle Scholar
  26. Matlock D, Ginsburg D, Paul V (1999) Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia 399:267–273Google Scholar
  27. 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 56:95–104CrossRefGoogle Scholar
  28. 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 109:399–407CrossRefGoogle Scholar
  29. 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 129:55–63CrossRefGoogle Scholar
  30. Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169CrossRefGoogle Scholar
  31. 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 1–37CrossRefGoogle Scholar
  32. Pedersén M, Collen J, Abrahamsson K, Ekdahl A (1996) Production of halocarbons from seaweeds: an oxidative stress reaction? Sci Mar 60:257–263Google Scholar
  33. 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 47:202–208CrossRefGoogle Scholar
  34. 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 128:161–170CrossRefGoogle Scholar
  35. Shibata T, Hama Y, Miyasaki T, Ito M, Nakamura T (2006) Extracellular secretion of phenolic substances from living brown algae. J Appl Phycol 18:787–794CrossRefGoogle Scholar
  36. Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defenses or valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612–618CrossRefGoogle Scholar
  37. Tuomi J (1992) Toward integration of plant defence theories. Trends Ecol Evol 7:365–367CrossRefGoogle Scholar
  38. 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 107:440–450CrossRefGoogle Scholar
  39. 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 42:1773–1779CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Environmental Science and Analytical ChemistryStockholm UniversityStockholmSweden
  2. 2.AquaBiota Water ResearchStockholmSweden

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