Skip to main content
Log in

Adsorbable organic bromine compounds (AOBr) in aquatic samples: a nematode-based toxicogenomic assessment of the exposure hazard

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Elevated levels of adsorbable organic bromine compounds (AOBr) have been detected in German lakes, and cyanobacteria like Microcystis, which are known for the synthesis of microcystins, are one of the main producers of natural organobromines. However, very little is known about how environmental realistic concentrations of organobromines impact invertebrates. Here, the nematode Caenorhabditis elegans was exposed to AOBr-containing surface water samples and to a Microcystis aeruginosa-enriched batch culture (MC-BA) and compared to single organobromines and microcystin-LR exposures. Stimulatory effects were observed in certain life trait variables, which were particularly pronounced in nematodes exposed to MC-BA. A whole genome DNA-microarray revealed that MC-BA led to the differential expression of more than 2000 genes, many of which are known to be involved in metabolic, neurologic, and morphologic processes. Moreover, the upregulation of cyp- and the downregulation of abu-genes suggested the presence of chronic stress. However, the nematodes were not marked by negative phenotypic responses. The observed difference in MC-BA and microcystin-LR (which impacted lifespan, growth, and reproduction) exposed nematodes was hypothesized to be likely due to other compounds within the batch culture. Most likely, the exposure to low concentrations of organobromines appears to buffer the effects of toxic substances, like microcystin-LR.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abebe E, Decraemer W, De Ley P (2008) Global diversity of nematodes (Nematoda) in freshwater. Hydrobiologia 595:67–78. doi:10.1007/s10750-007-9005-5

    Article  Google Scholar 

  • Andrassy I (1984) Klasse nematoda. Gustav Fischer Verlag, Stuttgart

    Google Scholar 

  • Andrianasolo EH, France D, Cornell-Kennon S, Gerwick WH (2006) DNA methyl transferase inhibiting halogenated monoterpenes from the Madagascar red marine alga Portieria hornemannii. J Nat Prod 69:576–579. doi:10.1021/np0503956

    Article  CAS  Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    CAS  Google Scholar 

  • Calabrese EJ (2010) Hormesis is central to toxicology, pharmacology and risk assessment. Hum Exp Toxicol 29:249–261. doi:10.1177/0960327109363973

    Article  Google Scholar 

  • Cedergreen N (2010) Predicting hormesis in mixtures. Integr Environ Assess Manag 6:310–311. doi:10.1002/ieam.41

    Article  Google Scholar 

  • Ciminiello P, Fattorusso E, Forino M, Di Rosa M, Ianaro A, Poletti R (2001) Structural elucidation of a new cytotoxin isolated from mussels of the Adriatic sea. J Org Chem 66:578–582. doi:10.1021/Jo001437s

    Article  CAS  Google Scholar 

  • Covich AP, Palmer MA, Crowl TA (1999) The role of benthic invertebrate species in freshwater ecosystems: zoobenthic species influence energy flows and nutrient cycling. Bioscience 49:119–127. doi:10.2307/1313537

    Article  Google Scholar 

  • Dalman MR, Deeter A, Nimishakavi G, Duan ZH (2012) Fold change and p-value cutoffs significantly alter microarray interpretations. BMC Bioinformatics 13(Suppl 2):S11. doi:10.1186/1471-2105-13-S2-S11

    Article  Google Scholar 

  • DIN (German Institute for Standardization) (2007) Water quality - determination of microcystins. Method using solid phase extraction (SPE) and high performance liquid chromatography (HPLC) with ultraviolet (UV) detection. ISO 20179:2007-10

  • Fuller RW, Cardellina JH, Kato Y, Brinen LS, Clardy J, Snader KM, Boyd MR (1992) A pentahalogenated monoterpene from the red alga Portieria hornemannii produces a novel cytotoxicity profile against a diverse panel of human tumor cell lines. J Med Chem 35:3007–3011. doi:10.1021/jm00094a012

    Article  CAS  Google Scholar 

  • Furhacker M, Scharf S, Weber H (2000) Bisphenol A: emissions from point sources. Chemosphere 41:751–756. doi:10.1016/S0045-6535(99)00466-X

    Article  CAS  Google Scholar 

  • Gribble GW (2004) Natural organohalogens: a new frontier for medicinal agents? J Chem Educ 81:1441–1449. doi:10.1021/ed081p1441

    Article  CAS  Google Scholar 

  • Gribble GW (2009) Naturally occurring organohalogen compounds: a comprehensive update, vol 91. Springer, Vienna

    Google Scholar 

  • Gribble GW (2012) Occurrence of halogenated alkaloids. Alkaloids Chem Biol 71:1–165. doi:10.1016/B978-0-12-398282-7.00001-1

    Article  CAS  Google Scholar 

  • Hirschmann H (1952) Die Nematoden der Wassergrenze mittel-fränkischer Gewässer. Zool Jb (Syst) 81:313–436

    Google Scholar 

  • Höss S, Haitzer M, Traunspurger W, Steinberg CEW (1999) Growth and fertility of Caenorhabditis elegans (nematoda) in unpolluted freshwater sediments: response to particle size distribution and organic content. Environ Toxicol Chem 18:2921–2925. doi:10.1002/etc.5620181238

    Article  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57. doi:10.1038/nprot.2008.211

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13. doi:10.1093/Nar/Gkn923

    Article  Google Scholar 

  • Hütteroth A (2006) Bildung organischer Bromverbindungen in Oberflächengewässern sowie Studien zum Verhalten während der Uferfiltration. PhD thesis (in German), Doktor der Naturwissenschaften, Technische Universität Berlin, Berlin

  • Hütteroth A, Putschew A, Jekel M (2007) Natural production of organic bromine compounds in Berlin lakes. Environ Sci Technol 41:3607–3612. doi:10.1021/es062384k

    Article  Google Scholar 

  • Ioannides C (2008) Cytochromes P450: role in the metabolism and toxicity of drugs and other xenobiotics, royal society of chemistry

  • Ju J, Lieke T, Saul N, Pu Y, Yin L, Kochan C, Putschew A, Baberschke N, Steinberg CE (2014a) Neurotoxic evaluation of two organobromine model compounds and natural AOBr-containing surface water samples by a Caenorhabditis elegans test. Ecotoxicol Environ Saf 104:194–201. doi:10.1016/j.ecoenv.2014.03.009

    Article  CAS  Google Scholar 

  • Ju J, Saul N, Steinberg CEW, Kochan C, Putschew A, Pu Y, Yin L (2014b) Cyanobacterial xenobiotics as evaluated by a novel Caenorhabditis elegans neurotoxicity screening test. Int J Environ Res Public Health 11:4589–4606. doi:10.3390/ijerph110504589

    Article  Google Scholar 

  • Kaletta T, Hengartner MO (2006) Finding function in novel targets: C. elegans as a model organism. Nat Rev Drug Discov 5:387–398. doi:10.1038/nrd2031

    Article  CAS  Google Scholar 

  • Kim SJ, Choung SY (2009) Whole genomic expression analysis of octachlorostyrene-induced chronic toxicity in Caenorhabditis elegans. Arch Pharm Res 32:1585–1592. doi:10.1007/s12272-009-2111-3

    Article  CAS  Google Scholar 

  • Kümmerer K (2001) Drugs in the environment: emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources—a review. Chemosphere 45:957–969. doi:10.1016/S0045-6535(01)00144-8

    Article  Google Scholar 

  • Kuniyoshi M, Yamada K, Higa T (1985) A biologically-active diphenyl ether from the green-alga Cladophora fascicularis. Experientia 41:523–524. doi:10.1007/Bf01966182

    Article  CAS  Google Scholar 

  • Law RJ, Allchin CR, de Boer J, Covaci A, Herzke D, Lepom P, Morris S, Tronczynski J, de Wit CA (2006) Levels and trends of brominated flame retardants in the European environment. Chemosphere 64:187–208. doi:10.1016/j.chemosphere.2005.12.007

    Article  CAS  Google Scholar 

  • Leung MCK, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, Meyer JN (2008) Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106:5–28. doi:10.1093/toxsci/kfn121

    Article  CAS  Google Scholar 

  • Li X, Ma J, Fang Q, Li Y (2013) Transcription alterations of microRNAs, cytochrome P4501A1 and 3A65, and AhR and PXR in the liver of zebrafish exposed to crude microcystins. Toxicon 73:17–22. doi:10.1016/j.toxicon.2013.07.002

    Article  CAS  Google Scholar 

  • Lieke T, Steinberg CEW, Ju J, Saul N (2015) Natural marine and synthetic xenobiotics get on nematode’s nerves: neuro-stimulating and neurotoxic findings in Caenorhabditis elegans. Mar Drugs 13:2785–2812. doi:10.3390/md13052785

    Article  CAS  Google Scholar 

  • Linington RG, Edwards DJ, Shuman CF, McPhail KL, Matainaho T, Gerwick WH (2008) Symplocamide A, a potent cytotoxin and chymotrypsin inhibitor from the marine cyanobacterium Symploca sp. J Nat Prod 71:22–27. doi:10.1021/Np070280x

    Article  CAS  Google Scholar 

  • Martins J, Oliva Teles L, Vasconcelos V (2007) Assays with Daphnia magna and Danio rerio as alert systems in aquatic toxicology. Environ Int 33:414–425. doi:10.1016/j.envint.2006.12.006

    Article  CAS  Google Scholar 

  • Maskey RP, Grun-Wollny I, Fiebig HH, Laatsch H (2002) Akashins A, B, and C: novel chlorinated indigoglycosides from Streptomyces sp GW 48/1497. Angew Chem Int Ed Engl 41:597–599. doi:10.1002/1521-3773(20020215)41:4<597::Aid-Anie597>3.0.Co;2-Z

    Article  CAS  Google Scholar 

  • Meinelt T, Schreckenbach K, Pietrock M, Heidrich S, Steinberg CEW (2008) Humic substances (review series). Part 1: dissolved humic substances (HS) in aquaculture and ornamental fish breeding. Environ Sci Pollut Res 15:17–22. doi:10.1065/espr2007.08.448

    Article  Google Scholar 

  • Menzel R, Bogaert T, Achazi R (2001) A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch Biochem Biophys 395:158–168. doi:10.1006/abbi.2001.2568

    Article  CAS  Google Scholar 

  • Menzel R, Rödel M, Kulas J, Steinberg CEW (2005) CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch Biochem Biophys 438:93–102. doi:10.1016/j.abb.2005.03.020

    Article  CAS  Google Scholar 

  • Menzel R, Swain SC, Höss S, Claus E, Menzel S, Steinberg CE, Reifferscheid G, Stürzenbaum SR (2009) Gene expression profiling to characterize sediment toxicity—a pilot study using Caenorhabditis elegans whole genome microarrays. BMC Genomics 10:160. doi:10.1186/1471-2164-10-160

    Article  Google Scholar 

  • Morita K, Chow KL, Ueno N (1999) Regulation of body length and male tail ray pattern formation of Caenorhabditis elegans by a member of TGF-beta family. Development 126:1337–1347

    CAS  Google Scholar 

  • Mulder C, Boit A, Bonkowski M, de Ruiter PC, Mancinelli G, van der Heijden MGA, van Wijnen HJ, Vonk JA, Rutgers M (2011) A belowground perspective on Dutch agroecosystems: how soil organisms interact to support ecosystem services. in: Guy W (Ed.). Advances in Ecological Research, Academic Press, pp. 277-357. doi: 10.1016/b978-0-12-374794-5.00005-5

  • Oleksy-Frenzel J, Wischnack S, Jekel M (2000) Application of ion-chromatography for the determination of the organic-group parameters AOCl, AOBr and AOI in water. Fresenius J Anal Chem 366:89–94. doi:10.1007/s002160050016

    Article  CAS  Google Scholar 

  • Peltonen J, Aarnio V, Heikkinen L, Lakso M, Wong G (2013) Chronic ethanol exposure increases cytochrome P-450 and decreases activated in blocked unfolded protein response gene family transcripts in Caenorhabditis elegans. J Biochem Mol Toxicol 27:219–228. doi:10.1002/jbt.21473

    Article  CAS  Google Scholar 

  • Pouria S, De Andrade A, Barbosa J, Cavalcanti RL, Barreto VTS, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA (1998) Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet 352:21–26. doi:10.1016/S0140-6736(97)12285-1

    Article  CAS  Google Scholar 

  • Rezanka T, Dembitsky VM (2003) Brominated oxylipins and oxylipin glycosides from Red Sea corals. Eur J Org Chem 2003:309–316. doi:10.1002/ejoc.200390034

    Article  Google Scholar 

  • Saul N, Baberschke N, Chakrabarti S, Stürzenbaum SR, Lieke T, Menzel R, Jonas A, Steinberg CE (2014a) Two organobromines trigger lifespan, growth, reproductive and transcriptional changes in Caenorhabditis elegans. Environ Sci Pollut Res Int 21:10419–10431. doi:10.1007/s11356-014-2932-6

    Article  CAS  Google Scholar 

  • Saul N, Chakrabarti S, Stürzenbaum SR, Menzel R, Steinberg CE (2014b) Neurotoxic action of microcystin-LR is reflected in the transcriptional stress response of Caenorhabditis elegans. Chem Biol Interact 223C:51–57. doi:10.1016/j.cbi.2014.09.007

    Article  Google Scholar 

  • Shaw SD, Blum A, Weber R, Kannan K, Rich D, Lucas D, Koshland CP, Dobraca D, Hanson S, Birnbaum LS (2010) Halogenated flame retardants: do the fire safety benefits justify the risks? Rev Environ Health 25:261–305. doi:10.1515/REVEH.2010.25.4.261

    Article  CAS  Google Scholar 

  • Shomar B (2007) Sources of adsorbable organic halogens (AOX) in sludge of Gaza. Chemosphere 69:1130–1135. doi:10.1016/j.chemosphere.2007.03.074

    Article  CAS  Google Scholar 

  • Simmons TL, Andrianasolo E, McPhail K, Flatt P, Gerwick WH (2005) Marine natural products as anticancer drugs. Mol Cancer Ther 4:333–342

    CAS  Google Scholar 

  • Steinberg CEW, Kamara S, Prokhotskaya VY, Manusadžianas L, Karasyova TA, Timofeyev MA, Jie Z, Paul A, Meinelt T, Farjalla VF, Matsuo AYO, Burnison BK, Menzel R (2006) Dissolved humic substances—ecological driving forces from the individual to the ecosystem level? Freshw Biol 51:1189–1210. doi:10.1111/j.1365-2427.2006.01571.x

    Article  CAS  Google Scholar 

  • Steinberg CEW, Meinelt T, Timofeyev MA, Bittner M, Menzel R (2008) Humic substances (review series). Part 2: interactions with organisms. Environ Sci Pollut Res 15:128–135. doi:10.1065/espr2007.07.434

    Article  Google Scholar 

  • Stewart I, Seawright AA, Shaw GR (2008) Cyanobacterial poisoning in livestock, wild mammals and birds—an overview. Adv Exp Med Biol 619:613–637. doi:10.1007/978-0-387-75865-7_28

    Article  CAS  Google Scholar 

  • Strange K, Christensen M, Morrison R (2007) Primary culture of Caenorhabditis elegans developing embryo cells for electrophysiological, cell biological and molecular studies. Nat Protoc 2:1003–1012. doi:10.1038/nprot.2007.143

    Article  CAS  Google Scholar 

  • Svircev Z, Baltic V, Gantar M, Jukovic M, Stojanovic D, Baltic M (2010) Molecular aspects of microcystin-induced hepatotoxicity and hepatocarcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 28:39–59. doi:10.1080/10590500903585382

    Article  CAS  Google Scholar 

  • Ura K, Kai T, Sakata S, Iguchi T, Arizono K (2002) Aquatic acute toxicity testing using the nematode Caenorhabditis elegans. J Health Sci 48:583–586

    Article  CAS  Google Scholar 

  • Urano F, Calfon M, Yoneda T, Yun C, Kiraly M, Clark SG, Ron D (2002) A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J Cell Biol 158:639–646. doi:10.1083/jcb.200203086

    Article  CAS  Google Scholar 

  • Wang L, Zou W, Zhong Y, An J, Zhang X, Wu M, Yu Z (2012) The hormesis effect of BDE-47 in HepG2 cells and the potential molecular mechanism. Toxicol Lett 209:193–201. doi:10.1016/j.toxlet.2011.12.014

    Article  CAS  Google Scholar 

  • Zullini A (1988) The ecology of the Lambro river. Riv Idrobiol 27:39–58

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Deutsche Forschungsgemeinschaft (DFG) grants STE 673/18, ME 2056/3 (RM) and PU 199/6-1 and King’s College London (SRS). Furthermore, we thank the Caenorhabditis Genetics Centre, which is funded by the National Institutes of Health National Centre for Research Resources, for the supply of the Caenorhabditis elegans strains and the King’s College London Genomics Centre for their support and access to microarray facilities. We declare that there is no conflict of interests and that the experiments comply with the current laws of the countries where the experiments were conducted.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nadine Saul.

Additional information

Responsible editor: Cinta Porte

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

(DOCX 17 kb)

Online Resource 2

(XLSX 150 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saul, N., Stürzenbaum, S.R., Chakrabarti, S. et al. Adsorbable organic bromine compounds (AOBr) in aquatic samples: a nematode-based toxicogenomic assessment of the exposure hazard. Environ Sci Pollut Res 22, 14862–14873 (2015). https://doi.org/10.1007/s11356-015-4694-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4694-1

Keywords

Navigation