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Two organobromines trigger lifespan, growth, reproductive and transcriptional changes in Caenorhabditis elegans

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Abstract

Organobromines of natural and artificial origin are omnipresent in aquatic and terrestrial environments. Although it is well established that exposure to high concentrations of organobromines are harmful to vertebrates, few studies have investigated the effect of environmentally realistic concentrations on invertebrates. Here, the nematode Caenorhabditis elegans was challenged with two organobromines, namely dibromoacetic acid (DBAA) and tetrabromobisphenol-A (TBBP), and monitored for changes in different life trait variables and global gene expression patterns. Fifty micromolar DBAA stimulated the growth and lifespan of the nematodes; however, the onset of reproduction was delayed. In contrast, TBBP changed the lifespan in a hormetic fashion, namely it was stimulated at 0.1 μM but impaired at 50 μM. The reproductive performance was even impaired at 2 μM TBBP. Moreover, DBAA could not reduce the toxic effect of TBBP when applied as a mixture. A whole-genome DNA microarray revealed that both organobromines curtailed signalling and neurological processes. Furthermore on the transcription level, 50 μM TBBP induced proteolysis and DBAA up-regulated biosynthesis and metabolism. To conclude, even naturally occurring concentrations of organobromines can influence the biomolecular responses and life cycle traits in C. elegans. The life extension is accompanied by negative changes in the reproductive behaviour, which is crucial for the stability of populations. Thus, this paper highlights that the effects of exposure to moderate, environmentally realistic concentrations of organobromines should not be ignored.

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References

  • Abbott AL (2011) Uncovering new functions for microRNAs in Caenorhabditis elegans. Curr Biol 21:R668–R671. doi:10.1016/j.cub.2011.07.027

    Article  CAS  Google Scholar 

  • Anderson GL, Boyd WA, Williams P (2001) Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ Toxicol Chem 20:833–838

    Article  CAS  Google Scholar 

  • Asplund G, Grimvall A (1991) Organohalogens in nature. Environ Sci Technol 25:1346–1350. doi:10.1021/Es00020a001

    Article  CAS  Google Scholar 

  • Bard SM (2000) Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquat Toxicol 48:357–389. doi:10.1016/S0166-445x(00)00088-6

    Article  CAS  Google Scholar 

  • Binns D, Dimmer E, Huntley R, Barrell D, O’Donovan C, Apweiler R (2009) QuickGO: a web-based tool for gene ontology searching. Bioinformatics 25:3045–3046. doi:10.1093/bioinformatics/btp536

    Article  CAS  Google Scholar 

  • Birnbaum LS, Staskal DF (2004) Brominated flame retardants: cause for concern? Environ Health Perspect 112:9–17

    Article  CAS  Google Scholar 

  • Bosch TCG, Krylow SM, Bode HR, Steele RE (1988) Thermotolerance and synthesis of heat-shock proteins—these responses are present in hydra-attenuata but absent in hydra-oligactis. Proc Natl Acad Sci U S A 85:7927–7931. doi:10.1073/pnas.85.21.7927

    Article  CAS  Google Scholar 

  • Braeckman BP, Houthoofd K, De Vreese A, Vanfleteren JR (2002) Assaying metabolic activity in ageing Caenorhabditis elegans. Mech Ageing Dev 123:105–119. doi:10.1016/S0047-6374(01)00331-1

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Broeks A, Janssen HW, Calafat J, Plasterk RH (1995) A P-glycoprotein protects Caenorhabditis elegans against natural toxins. EMBO J 14(9):1858–1866

    CAS  Google Scholar 

  • Broeks A, Gerrard B, Allikmets R, Dean M, Plasterk RH (1996) Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J 15:6132–6143

    CAS  Google Scholar 

  • Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 27:1451–1474. doi:10.1897/07-541

    Article  CAS  Google Scholar 

  • Covaci A, Voorspoels S, Abdallah MA, Geens T, Harrad S, Law RJ (2009) Analytical and environmental aspects of the flame retardant tetrabromobisphenol-A and its derivatives. J Chromatogr A 1216:346–363. doi:10.1016/j.chroma.2008.08.035

    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

    Article  Google Scholar 

  • Cypser JR, Tedesco P, Johnson TE (2006) Hormesis and aging in Caenorhabditis elegans. Exp Gerontol 41:935–939

    Article  CAS  Google Scholar 

  • de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12:833–845. doi:10.1038/Nrg3055

    Google Scholar 

  • Doonan R, McElwee JJ, Matthijssens F, Walker GA, Houthoofd K, Back P, Matscheski A, Vanfleteren JR, Gems D (2008) Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22:3236–3241

    Article  CAS  Google Scholar 

  • Drewes JE, Jekel M (1998) Behavior of DOC and AOX using advanced treated wastewater for groundwater recharge. Water Res 32:3125–3133. doi:10.1016/S0043-1354(98)00064-5

    Article  CAS  Google Scholar 

  • Echigo S, Itoh S, Natsui T, Araki T, Ando R (2004) Contribution of brominated organic disinfection by-products to the mutagenicity of drinking water. Water Sci Technol 50:321–328

    CAS  Google Scholar 

  • Engert A, Chakrabarti S, Saul N, Bittner M, Menzel R, Steinberg CEW (2013) Interaction of temperature and an environmental stressor: Moina macrocopa responds with increased body size, increased lifespan, and increased offspring numbers slightly above its temperature optimum. Chemosphere 90:2136–2141. doi:10.1016/j.chemosphere.2012.10.099

    Article  CAS  Google Scholar 

  • Fukuda N, Ito Y, Yamaguchi M, Mitumori K, Koizumi M, Hasegawa R, Kamata E, Ema M (2004) Unexpected nephrotoxicity induced by tetrabromobisphenol A in newborn rats. Toxicol Lett 150:145–155. doi:10.1016/j.toxlet.2004.01.001

    Article  CAS  Google Scholar 

  • Fuller RW, Cardellina JH 2nd, Jurek J, Scheuer PJ, Alvarado-Lindner B, McGuire M, Gray GN, Steiner JR, Clardy J, Menez E et al (1994) Isolation and structure/activity features of halomon-related antitumor monoterpenes from the red alga Portieria hornemannii. J Med Chem 37:4407–4411

    Article  CAS  Google Scholar 

  • Fürhacker M, Scharf S, Weber H (2000) Bisphenol A: emissions from point sources. Chemosphere 41:751–756

    Article  Google Scholar 

  • Gellert G (2000) Relationship between summarizing chemical parameters like AOX, TOC, TNb, and toxicity tests for effluents from the chemical production. Bull Environ Contam Toxicol 65:508–513

    Article  CAS  Google Scholar 

  • Gellner K, Praetzel G, Bosch TCG (1992) Cloning and expression of a heat-inducible hsp70 gene in 2 species of hydra which differ in their stress response. Eur J Biochem 210:683–691. doi:10.1111/j.1432-1033.1992.tb17469.x

    Article  CAS  Google Scholar 

  • Gerisch B, Weitzel C, Kober-Eisermann C, Rottiers V, Antebi A (2001) A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 1:841–851

    Article  CAS  Google Scholar 

  • Gribble GW (1999) The diversity of naturally occurring organobromine compounds. Chem Soc Rev 28:335–346. doi:10.1039/A900201d

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gribble GW (2010) Naturally occurring organohalogen compounds: a comprehensive update, vol 91. Springer, Vienna, New York

  • Gribble GW (2012) Occurrence of halogenated alkaloids. Alkaloids Chem Biol 71:1–165

    Article  CAS  Google Scholar 

  • Harrington LA, Harley CB (1988) Effect of vitamin E on lifespan and reproduction in Caenorhabditis elegans. Mech Ageing Dev 43:71–78

    Article  CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052. doi:10.1111/j.1365-313X.2010.04124.x

    Article  CAS  Google Scholar 

  • Hofmann S, Timofeyev MA, Putschew A, Menzel R, Steinberg CEW (2012) Leaf litter leachates have the potential to increase lifespan, body size, and offspring numbers in a clone of Moina macrocopa Straus. Chemosphere 86:883–890. doi:10.1016/j.chemosphere.2011.10.041

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009a) 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 

  • Huang DW, Sherman BT, Lempicki RA (2009b) 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 

  • 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 

  • James CE, Davey MW (2009) Increased expression of ABC transport proteins is associated with ivermectin resistance in the model nematode Caenorhabditis elegans. Int J Parasitol 39:213–220. doi:10.1016/j.ijpara.2008.06.009

    CAS  Google Scholar 

  • Jia K, Chen D, Riddle DL (2004) The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 131:3897–3906

    Article  CAS  Google Scholar 

  • Johnson TE, Henderson S, Murakami S, de Castro E, de Castro SH, Cypser J, Rikke B, Tedesco P, Link C (2002) Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J Inherit Metab Dis 25:197–206

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Keppler C, Ringwood AH (2001) Expression of P-glycoprotein in the gills of oysters, Crassostrea virginica: seasonal and pollutant related effects. Aquat Toxicol 54:195–204. doi:10.1016/S0166-445x(01)00151-5

    Article  CAS  Google Scholar 

  • Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304

    Article  CAS  Google Scholar 

  • Kirkwood TBL (1988) The nature and causes of ageing. Ciba Found Symp 134:193–207

    CAS  Google Scholar 

  • Krasner S, Chinn R, Pastor S, Sclimenti M, Weinberg H, Onstad G, Richardson S (2002) The occurrence of disinfection by-products of health concern in drinking water. Epidemiology 13:S108

    Google Scholar 

  • Kuiper RV, van den Brandhof EJ, Leonards PE, van der Ven LT, Wester PW, Vos JG (2007) Toxicity of tetrabromobisphenol A (TBBPA) in zebrafish (Danio rerio) in a partial life-cycle test. Arch Toxicol 81:1–9. doi:10.1007/s00204-006-0117-x

    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 

  • Lee CK, Klopp RG, Weindruch R, Prolla TA (1999) Gene expression profile of aging and its retardation by caloric restriction. Science 285:1390–1393. doi:10.1126/science.285.5432.1390

    Article  CAS  Google Scholar 

  • Leri AC, Myneni SCB (2012) Natural organobromine in terrestrial ecosystems. Geochim Cosmochim Acta 77:1–10. doi:10.1016/j.gca.2011.11.012

    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 

  • Linder RE, Klinefelter GR, Strader LF, Suarez JD, Dyer CJ (1994) Acute spermatogenic effects of bromoacetic acids. Fundam Appl Toxicol 22:422–430

    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 

  • Liu S, Saul N, Pan B, Menzel R, Steinberg CE (2013) The non-target organism Caenorhabditis elegans withstands the impact of sulfamethoxazole. Chemosphere 93:2373–2380. doi:10.1016/j.chemosphere.2013.08.036

    Article  CAS  Google Scholar 

  • Loos R, Barcelo D (2001) Determination of haloacetic acids in aqueous environments by solid-phase extraction followed by ion-pair liquid chromatography-electrospray ionization mass spectrometric detection. J Chromatogr A 938:45–55. doi:10.1016/S0021-9673(01)01092-5

    Article  CAS  Google Scholar 

  • Manninen PKG, Hasanen E (1992) Total organochlorine and organobromine in Finnish water courses. Hydrobiologia 243:475–479. doi:10.1007/Bf00007065

    Article  Google Scholar 

  • Melnick RL, Nyska A, Foster PM, Roycroft JH, Kissling GE (2007) Toxicity and carcinogenicity of the water disinfection byproduct, dibromoacetic acid, in rats and mice. Toxicology 230:126–136. doi:10.1016/j.tox.2006.11.006

    Article  CAS  Google Scholar 

  • Mohideen SS, Ichihara S, Banu S, Liu F, Kitoh J, Ichihara G (2009) Changes in neurotransmitter receptor expression levels in rat brain after 4-week exposure to 1-bromopropane. Neurotoxicology 30:1078–1083. doi:10.1016/j.neuro.2009.06.007

    Article  CAS  Google Scholar 

  • Muñoz MJ, Riddle DL (2003) Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity. Genetics 163:171–180

    Google Scholar 

  • Pacifici RE, Davies KJA (1990) Protein-degradation as an index of oxidative stress. Methods Enzymol 186:485–502

    Article  CAS  Google Scholar 

  • Prince EK, Pohnert G (2010) Searching for signals in the noise: metabolomics in chemical ecology. Anal Bioanal Chem 396:193–197. doi:10.1007/s00216-009-3162-5

    Article  CAS  Google Scholar 

  • Putri SP, Nakayama Y, Matsuda F, Uchikata T, Kobayashi S, Matsubara A, Fukusaki E (2013) Current metabolomics: practical applications. J Biosci Bioeng 115:579–589. doi:10.1016/j.jbiosc.2012.12.007

    Article  CAS  Google Scholar 

  • Putschew A, Mania M, Jekel M (2003) Occurrence and source of brominated organic compounds in surface waters. Chemosphere 52:399–407. doi:10.1016/S0045-6535(03)00195-4

    Article  CAS  Google Scholar 

  • Roff D (2001) Age and size at maturity. In: Evolutionary ecology: concepts and case studies. Oxford University Press, Oxford, pp 99–112

  • Roh J-Y, Jung I-H, Lee J-Y, Choi J (2007) Toxic effects of di (2-ethylhexyl) phthalate on mortality, growth, reproduction and stress-related gene expression in the soil nematode Caenorhabditis elegans. Toxicology 237:126–133

    Article  CAS  Google Scholar 

  • Saul N, Pietsch K, Sturzenbaum SR, Menzel R, Steinberg CE (2013) Hormesis and longevity with tannins: free of charge or cost-intensive? Chemosphere 93:1005–1008. doi:10.1016/j.chemosphere.2013.05.069

    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 

  • Smital T, Sauerborn R, Pivcevic B, Krca S, Kurelec B (2000) Interspecies differences in P-glycoprotein mediated activity of multixenobiotic resistance mechanism in several marine and freshwater invertebrates. Comp Biochem Physiol C 126:175–186. doi:10.1016/S0742-8413(00)00110-9

    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 

  • Sun YX, Gu P (2007) Determination of haloacetic acids in hospital effluent after chlorination by ion chromatography. J Environ Sci (China) 19:885–891

    Article  CAS  Google Scholar 

  • Wang H, Wick RL, Xing B (2009) Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut 157:1171–1177. doi:10.1016/j.envpol.2008.11.004

    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 

  • Zhang BH, Wang QL, Pan XP (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289. doi:10.1002/Jcp.20869

    Article  CAS  Google Scholar 

  • Zhang XL, Luo XJ, Chen SJ, Wu JP, Mai BX (2009) Spatial distribution and vertical profile of polybrominated diphenyl ethers, tetrabromobisphenol A, and decabromodiphenylethane in river sediment from an industrialized region of South China. Environ Pollut 157:1917–1923. doi:10.1016/j.envpol.2009.01.016

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Deutsche Forschungsgemeinschaft (DFG) grants STE 673/18 and ME 2056/3 (RM), 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 also thank the anonymous reviewers for their valuable comments leading to the improvement of our paper. 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.

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  1. Department of Biology, Freshwater and Stress Ecology, Humboldt-Universität zu Berlin, Späthstr. 80/81, 12437, Berlin, Germany

    Nadine Saul, Nora Baberschke, Shumon Chakrabarti, Thora Lieke, Ralph Menzel & Christian E. W. Steinberg

  2. School of Biomedical Sciences, Analytical and Environmental Sciences Division, King’s College London, 150 Stamford Street, London, SE1 9NH, UK

    Stephen R. Stürzenbaum

  3. RECETOX, Faculty of Science, Masaryk University, Kamenice 753/5, 62500, Brno, Czech Republic

    Adam Jonáš

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OR 1

Efficiency of each primer pair, primer sequences and annealing temperatures (PDF 148 kb)

OR 2

qRT-PCR results (PDF 234 kb)

OR 3

Full list and graph of DBAA-related GO terms (XLSX 622 kb)

OR 4

Full list and graph of TBBP-related GO terms (XLSX 308 kb)

OR 5

Full list of DEGs and their fold change (XLSX 80 kb)

OR 6

Raw microarray data and normalised values (XLSX 15678 kb)

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Saul, N., Baberschke, N., Chakrabarti, S. et al. Two organobromines trigger lifespan, growth, reproductive and transcriptional changes in Caenorhabditis elegans . Environ Sci Pollut Res 21, 10419–10431 (2014). https://doi.org/10.1007/s11356-014-2932-6

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