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High estradiol exposure disrupts the reproductive cycle of the clam Ruditapes decussatus in a sex-specific way

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Abstract

Bivalve species may be susceptible to environmental estrogenic compounds including estradiol (E2). However, they are able to biotransform the hormone quite readily and inactivate its estrogenic action. To study the long-term effects of elevated free E2 tissue levels, we transiently exceeded the biotransformation capacity of the clam Ruditapes decussatus by exposing them with high E2 concentrations (400 ng/L) and subsequently study the consequences on gametogenesis during the following reproductive cycle. Exposure to 400 ngE2/L led to a significant increase in tissue free E2 levels, which reached 10–50 ng E2Eq/gww. No deleterious effect on gonado-somatic index (GSI), condition index (CI), or ability to respond to the stress on stress test could be detected after a month of exposure, suggesting the absence of negative effects on the clam’s health. However, a marked increase in gametogenesis could be observed in both sexes during the exposure. Subsequent transplantation of the clams in the field allowed the normal development of the male clams and maturation of the gonads without any detrimental effect observed after 4 months. In contrast, in early July, all female clams formerly exposed to E2 showed lower health status, and only ovaries with atretic oocytes while all control and indigenous females were normal and mature. These results show a sex-specific effect of high E2 exposure and suggest either a direct or indirect role for E2 in R. decussatus’ reproduction.

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References

  • Arcand-Hoy LD, Nimrod AC, Benson WH (1998) Endocrine-modulating substances in the environment: estrogenic effects of pharmaceutical products. Int J Toxicol 17:139–158

    Article  CAS  Google Scholar 

  • Atkinson S, Atkinson MJ, Tarrant AM (2003) Estrogens from sewage in coastal marine environments. Environ Health Perspect 111:531–535

    Article  CAS  Google Scholar 

  • Bannister R, Beresford N, Granger DW, Pounds NA, Rand-Weaver M, White R, Jobling S, Routledge EJ (2013) No substantial changes in estrogen receptor and estrogen-related receptor orthologue gene transcription in Marisa cornuarietis exposed to estrogenic chemicals. Aquat Toxicol 140:19–26

    Article  CAS  Google Scholar 

  • Baronti C, Curini R, D’Ascenzo G, Di Corcia A, Gentili A, Samperi R (2000) Monitoring natural and synthetic estrogens at activated treatment plants and in receiving river water. Environ Sci Technol 34:5059–5066

    Article  CAS  Google Scholar 

  • Borg W, Shackleton C, Pahuja SL, Hochburg RB (1995) Long-lived testosterone esters in the rat. Proc Natl Acad Sci U S A 92:1545–1549

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A dye binding assay for protein. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Ciocan CM, Cubero-Leon E, Puinean AM, Hill EM, Minier C, Osada M, Fenlon K, Rotchell JM (2010) Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis. Environ Pollut 158:2977–2984

    Article  CAS  Google Scholar 

  • Ciocan C, Cubero-Leon E, Minier C, Rotchell JM (2011) Identification of reproduction-specific genes associated with maturation and estrogen exposure in a marine bivalve Mytilus edulis. Plos One 6(7):e22326. https://doi.org/10.1371/journal.pone.0022326

    Article  CAS  Google Scholar 

  • COM (2012) Directive of the European Parliament and of the Council amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. COM 2011:876

    Google Scholar 

  • Cubero-Leon E, Ciocan CM, Hill EM, Osada M, Kishida M, Itoh N, Kondo R, Minier C, Rotchell J (2010) Estrogens disrupt serotonin receptor and cyclooxygenase gene expression in the gonads of mussels (Mytilus edulis). Aquat Toxicol 98:178–187

    Article  CAS  Google Scholar 

  • Cubero-Leon E, Minier C, Rotchell J, Hill EM (2011) Reference gene selection for qPCR in mussel, Mytilus edulis, during gametogenesis and exogenous estrogen exposure. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-012-0772-9

  • Cubero-Leon E, Minier C, Rotchell J, Hill EM (2012) Metabolomic analysis of sex specific metabolites in gonads of the mussel, Mytilus edulis. Comp Biochem Physiol D7:212–219

    Google Scholar 

  • Denier X, Hill EM, Rotchell J, Minier C (2009) Estrogenic activity of cadmium, copper and zinc in the yeast-estrogen screen. Toxicol in Vitro 23:569–573

    Article  CAS  Google Scholar 

  • Desbrow C, Routledge EJ, Brighty GC, Sumpter JP, Waldock M (1998) Identification of estrogenic chemicals in STW effluent. I: chemical fractionation and in vitro biological screening. Environ Sci Technol 32:1549–1558

    Article  CAS  Google Scholar 

  • Forbes VE, Aufderheide J, Warbritton R, van der Hoeven N, Caspers N (2007) Does bisphenol A induce superfeminization in Marisa cornuarietis? Part II: toxicity test results and requirements for statistical power analyses. Ecotoxicol Environ Saf 66:319–325

    Article  CAS  Google Scholar 

  • Fossi-Tankoua O, Amiard-Triquet C, Denis F, Minier C, Mouneyrac C, Berthet B (2012) Physiological status and intersex in the endobenthic bivalve Scrobicularia plana from thirteen estuaries in northwest France. Environ Pollut 167:70–77

    Article  CAS  Google Scholar 

  • Frings CS, Fendley TW, Dunn RT, Queen CA (1972) Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chern 18:673

    CAS  Google Scholar 

  • Gagné F, Blaise C, Pellerin J, Pelletier E, Douville M, Gauthier-Clerc S, Viglino L (2003) Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comp Biochem Physiol C 134:189–198

    Article  Google Scholar 

  • Gagné F, Burgeot T, Hellou J, St-Jean S, Farcy E, Blaise C (2008) Spatial variations in biomarkers of Mytilus edulis mussels at four polluted regions spanning the Northern Hemisphere. Environ Res 107:201–217

    Article  CAS  Google Scholar 

  • Giusti A, Joaquim-Justo C (2013) Esterification of vertebrate like steroids in molluscs: a target of endocrine disruptors? Comp Biochem Physiol C158:187–198

    Google Scholar 

  • Gooding MP, Wilson VS, Folmar LC, Marcovich DT, Le Blanc GA (2003) The biocide tributyltin reduces the retention of testosterone as fatty acid ester in the mud snail (Iyanassa Obsoleta). Environ Health Perspect 111:426–430

    Article  CAS  Google Scholar 

  • Grant A, Tyler PA (1983) The analysis of data in studies of invertebrate reproduction. I: introduction and statistical analysis of gonad indices and maturity indices. Int J Invertebr Reprod 6:259–269

    Article  Google Scholar 

  • Hamza-Chaffai A (2013) Estrogenic endocrine disruptors and their possible deleterious effects on marine organisms: use of a novel monitoring bioassay. Int J Biotech Well Ind 2:1–9

    CAS  Google Scholar 

  • Janer G, Porte C (2007) Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates. Ecotoxicology 16:145–160

    Article  CAS  Google Scholar 

  • Janer G, Lavado R, Thibaut R, Porte C (2004a) Effects of 17β-estradiol exposure in the mussel Mytilus galloprovincialis. Mar Environ Res 58:443–446

    Article  CAS  Google Scholar 

  • Janer G, Mesia-Vela S, Porte C, Kauffman FC (2004b) Esterification of vertebrate-type steroids in the eastern oyster (Crassostrea virginica). Steroids 69:129–136

    Article  CAS  Google Scholar 

  • Janer G, Lavado R, Thibaut R, Porte C (2005) Effects of 17beta-estradiol exposure in the mussel Mytilus galloprovincialis: a possible regulating role for steroid acyltransferases. Aquat Toxicol 75:32–42

    Article  CAS  Google Scholar 

  • Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506

    Article  CAS  Google Scholar 

  • Johnson AC, Belfroid A, DiCorcia A (2000) Estimating steroid oestrogen inputs into activated sludge treatment works and observations on their removal from the effluent. Sci Total Environ 256:163–173

    Article  CAS  Google Scholar 

  • Keay J, Bridgham JT, Thornton JW (2006) The Octopus vulgaris estrogen receptors a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 147:3861–3869

    Article  CAS  Google Scholar 

  • Ketata I, Guermazi F, Rebai T, Hamza-Chaffai A (2007a) Variation of steroid concentrations during the reproductive cycle of the clam Ruditapes decussatus: a one year study in the gulf of Gabès area. Comp Biochem Physiol 147(A):424–431

    Article  CAS  Google Scholar 

  • Ketata I, Smaoui-Damak W, Guermazi F, Rebai T, Hamza-Chaffai A (2007b) In situ endocrine disrupting effects of cadmium on the reproduction of Ruditapes decussatus. Comp Biochem Physiol 147 A: 424–431

  • Ketata I, Denier X, Hamza-Chaffai A, Minier C (2008) Endocrine-related reproductive effects in molluscs. Comp Biochem Physiol 147(C):261–270

    Google Scholar 

  • Kuch HM, Ballschmitter K (2001) Determination of endocrine-disrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCI)-MS in the picogram per liter range. Environ Sci Technol 35:320–326

    Article  CAS  Google Scholar 

  • Labadie P, Peck M, Minier C, Hill EM (2007) Identification of the steroid fatty acid ester conjugates formed in vivo in Mytilus edulis as a result of exposure to estrogens. Steroids 72:41–49

    Article  CAS  Google Scholar 

  • Langston WJ, Burt GR, Chesman BS (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Mar Ecol Prog Ser 333:173–184

    Article  CAS  Google Scholar 

  • Lavado R, Janer G, Pate G (2006) Steroid levels and steroid metabolism in the mussel Mytilus edulis: the modulating of dispersed crude oil and alkylphenol. Aqua Toxicol 79:65–72

    Article  CAS  Google Scholar 

  • Legler JJ, Leonards P, Spenkelink A, Murk AJ (2003) In vitro biomonitoring in polar extracts of solid phase matrices reveals the presence of unknown compounds with estrogenic activity. Ecotoxicology 12:239–249

    Article  CAS  Google Scholar 

  • Li Q, Osada M, Suzuki T, Mori K (1998) Changes in vitellin during oogenesis and effect of estradiol-17β on vitellogenesis in the Pacific oyster Crassostrea gigas. Invertebr Reprod Dev 33:87–93

    Article  Google Scholar 

  • Lobel PB, Bajdik CD, Belkhode SP, Jackson SE, Longerich HP (1991) Improved protocol for collecting mussel watch specimens taking into account sex, size, condition, shell shape and chronological age. Arch Environ Contam Toxicol 21:409–414

    Article  Google Scholar 

  • Matthiessen P, Arnold D, Johnson AC, Pepper TJ, Pottinger TG, Pulman KGT (2006) Contamination of headwater streams in the United Kingdom by oestrogenic hormones from livestock farms. Sci Tot Environ 367:616–630

    Article  CAS  Google Scholar 

  • Mori K, Muramatsu T, Nakamura Y (1972) Effects of steroids on oyster-V. Acceleration of glycogenolysis in female Crassostrea gigas by estradiol-17b injection under natural conditions. Bull Jpn Soc Sci Fish 38:1185–1189

    Article  CAS  Google Scholar 

  • Oehlmann J, Schulte-Oehlmann U, Tillmann M, Markert B (2000) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: bisphenol-A and octylphenol as xeno-estrogens. Ecotoxicology 9:383–397

    Article  CAS  Google Scholar 

  • Peck MR, Labadie P, Minier C, Hill EM (2007) Profiles of environmental and endogenous estrogens in the zebra mussel Dreissena polymorpha. Chemosphere 69:1–8

    Article  CAS  Google Scholar 

  • Purdom CE, Hardiman PA, Bye VJ, Eno NC, Tyler CR, Sumpter JP (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8:275–285

    Article  CAS  Google Scholar 

  • Quinn B, Gagné F, Costello M, McKenzie C, Wilson J, Mothersill C (2004) The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquat Toxicol 66:279–292

    Article  CAS  Google Scholar 

  • Rodgers-Gray TP, Jobling S, Morris S, Kelly C, Kirby S, Janbakhsh A, Harries JE, Waldock MJ, Sumpter JP, Tyler CR (2000) Long-term temporal changes in the estrogenic composition of treated sewage effluent and its biological effects on fish. Environ Sci Technol 34:1521–1528

    Article  CAS  Google Scholar 

  • Routledge EJ, Sumpter JP (1996) Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ Toxicol Chem 15:241–248

    Article  CAS  Google Scholar 

  • Sasaki T, Matsy S, Sorae A (1972) Effect of acetic acid concentration on the colour reaction in the O-toluidine boric acid method for blood glucose estimation. Rinsho Kagarku 1:346–353

    CAS  Google Scholar 

  • Scott AP (2013) Do mollusks use vertebrate sex steroids as reproductive hormones? II. Critical review of the evidence that steroids have biological effects. Steroids 78:268–281

    Article  CAS  Google Scholar 

  • Seemann F, Knigge TA, Rocher B, Minier C, Monsinjon T (2013) 17β-Estradiol induces changes in cytokine levels in head kidney and blood of juvenile sea bass (Dicentrarchus labrax, L. 1758). Mar Environ Res 87-88:44–51

    Article  CAS  Google Scholar 

  • Shore LS, Gurevitz M, Shemesh M (1993) Estrogen as an environmental pollutant. Bull Environ Contam Toxicol 51:361–366

    Article  CAS  Google Scholar 

  • Smaoui-Dammak W (2005) Effets de la contamination in situ (Golfe de Gabes) par le cadmium sur la synthèse des métallothionéines et sur le potentiel reproducteur de la palourde Ruditapes decussatus. PhD thesis, Sfax University, Tunisia, 226 pp

  • Smaoui-Dammak W, Mathieu M, Rebai T, Hamza-Chaffai A (2007) Histology of the reproductive tissue of the clam Ruditapes decussatus from the Gulf of Gabes (Tunisia). Invertebr Reprod Dev 503:117–126

    Article  Google Scholar 

  • Stanton MG (1968) Colorimetric determination of inorganic phosphate in the presence of biological material and adenosine triphosphate. Anal Biochem 22:27–34

    Article  CAS  Google Scholar 

  • Strott CA (1996) Steroid Sulfotransferases. Endocr Rev 1:670–697

    Article  Google Scholar 

  • Tashiro Y, Takemura A, Fujii H, Takahira K, Nakanishi Y (2003) Livestock wastes as a source of estrogens and their effects on wildlife of Manko tidal flat, Okinawa. Mar Poll Bull 47:143–147

    Article  CAS  Google Scholar 

  • Ternes TA, Stumpf M, Mueller J, Haberer K, Wilken RD, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants. I: investigations in Germany, Canada and Brazil. Sci Total Environ 225:81–90

    Article  CAS  Google Scholar 

  • Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714–1717

    Article  CAS  Google Scholar 

  • Tyler CR, Joling S (2008) Roach, sex and gender-bending chemicals: the feminization of wild fish in English rivers. Bioscience 58(11):1051–1059

    Article  Google Scholar 

  • Viarengo A, Canesi L, Pertica M, Mancinelli G, Accomando R, Smaal AC, Orunesua M (1995) Stress on stress response: a simple monitoring tool in the assessment of a general stress syndrome in mussels marine. Environ Res 39:245–248

    CAS  Google Scholar 

  • Wang C, Croll RP (2004) Effects of sex steroids on gonadal development and gender determination in the sea scallop, Placopecten magellanicus. Aquaculture 238:483–498

    Article  CAS  Google Scholar 

  • Ying GG, Kookana RS, Ru YJ (2002) Occurrence and fate of hormone steroids in the environment. Environ Interna 28:545–551

    Article  CAS  Google Scholar 

  • Zamouri-Langar N, Chouba L, Jarboui O, Mrabet R (2006) Présence du bivalve veneridae Ruditapes philippinarum (Adams and Reeve, 1850) sur le littoral sud de la Tunisie. Bull Inst Natn Scien Tech Mer de Salammbô 33:23–27

    Google Scholar 

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Acknowledgments

Special thanks are due to Kristell Kelner from the BioMEA research unit in Caen (France) for her valuable help in histological analyses. Christophe Minier was funded by the European Regional Development Fund in the framework of the INTERREG IV A France (Channel)—England program (DIESE project, #4040).

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Correspondence to Sawssan Mezghani-Chaari.

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Responsible editor: Philippe Garrigues

Highlights

• Exposure to high E2 concentration disrupts the clam’s ability to maintain the free E2 to low level.

• Exposure to high E2 concentration does not affect survival or CI during exposure of the clams.

• Transient exposure to high E2 concentration affects the reproductive cycle of female but not of male clams.

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Mezghani-Chaari, S., Machreki-Ajimi, M., Hamza-Chaffai, A. et al. High estradiol exposure disrupts the reproductive cycle of the clam Ruditapes decussatus in a sex-specific way. Environ Sci Pollut Res 24, 26670–26680 (2017). https://doi.org/10.1007/s11356-017-0146-4

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  • DOI: https://doi.org/10.1007/s11356-017-0146-4

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