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Journal of Soils and Sediments

, Volume 15, Issue 2, pp 445–455 | Cite as

Probing the xeno-oestrogenic impact of sediment cores contaminated by the pulp and paper industry: induction of aromatase cyp19a1b in late larval zebrafish

  • Tarini P. Sahoo
  • Aimo Oikari
Sediments, Sec 1 • Sediment Quality and Impact Assessment • Research Article
  • 144 Downloads

Abstract

Purpose

Chemicals in effluents from the wood industry have been widely identified as sources of contamination affecting endocrine function in aquatic animals. This study examined the changes in transcript levels of key biomarkers, cytochrome P450 1A (cyp1a), brain aromatase (cyp19a1b) and vitellogenin 1 (vtg1), in late larval zebrafish exposed to sediment cores from areas upstream and downstream (two distances) from a pulp and paper mill in Finland.

Materials and methods

Bioluminescence inhibition of Vibrio fischeri by sediment elutriates was measured to determine the overall toxicity of the sediment. Then, a whole-sediment bioassay with 20-day post-fertilization zebrafish (20dpfZF) to lake sediment (0–5-cm and 20–30-cm layers) was conducted for 3 days, and changes in cyp1a, cyp19a1b and vtg1transcript levels were assessed using quantitative reverse transcription PCR (qRT-PCR) analyses.

Results and discussion

Lack of inhibition of bacterial (V. fischeri) bioluminescence by sediment elutriates indicated the non-toxic nature of the samples. Changes in gene expression of cyp19a1b (P < 0.001), but not of cyp1a and vtg1 as measured by qRT-PCR, suggested oestrogenic impact of the industrial contaminated sediment on the steroidogenic pathway of the fish. While aromatase played a significant role, more specifically for both the sites 1 and 3 km downstream, the upper layers (0–5 cm) showed higher upregulation of cyp19a1b compared to the reference sediment located 9 km upstream from the mill. There was a significantly higher upregulation of cyp19a1b (P = 0.001) by 0–5 cm compared to the that at the 20–30-cm layer at the 1-km site, indicating an oestrogenic impact of recent surface sediment near the mill compared to that in the site further downstream.

Conclusions

These results highlight the toxic potential of the pulp mill-contaminated sediment to aquatic biota, indicated by oestrogen-responsive cyp19a1b regulation in an immature fish (20dpfZF). 

Keywords

cyp19a1b Oestrogenicity PPME qRT-PCR vtg1 Whole-sediment bioassay Zebrafish 

Notes

Acknowledgments

We thank Dr. Aarno Karels for help with collection of sediments in Southern Lake Saimaa. The authors also thank Mervi Koistonen for help with sediment processing and experimentation, and Dr. Eeva-Riikka Vehniäinen for numerous technical advices. Dr. Tuula Sinisalo is thanked for help with the TOC analysis. We would also like to thank the anonymous reviewers for their valuable suggestions to strengthen this paper.

Supplementary material

11368_2014_1043_MOESM1_ESM.docx (37 kb)
ESM 1 (DOCX 37 kb)

References

  1. Ahokas JT, Karki NT, Oikari A, Soivio A (1976) Mixed function mono-oxygenase of fish as an indicator of pollution of aquatic environments by industrial effluent. Bull Environ Contam Toxicol 16:270–274CrossRefGoogle Scholar
  2. Ankley G, Mihaich E, Stahl R, Tillitt D, Colborn T, McMaster S, Miller R, Bantle J, Campbell P, Denslow N, Dickerson R, Folmar L, Fry M, Giesy J, Gray LE, Guiney P, Hutchinson T, Kennedy S, Kramer V, LeBlanc G, Mayes M, Nimod A, Patino R, Peterson R, Purdy R, Ringer R, Thomas P, Touart L, Van Der Kraak G, Zacharewski T (1998) Overview of a workshop on screening methods for detecting potential (anti-) estrogenic/androgenic chemicals in wildlife. Environ Toxicol Chem 17:68–87CrossRefGoogle Scholar
  3. Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrrano JA, Tietge JE, Villeneuve DL (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730–741CrossRefGoogle Scholar
  4. Billiard SM, Hahn ME, Franks DG, Peterson RE, Bols NC, Hodson PV (2002) Binding of polycyclic aromatic hydrocarbons (PAHs) to teleost aryl hydrocarbon receptors (AHRs). Comp Biochem Physiol B 133:55–68CrossRefGoogle Scholar
  5. Brinkworth LC, Hodson PV, Tabash S, Lee P (2003) CYP1A induction and blue sac disease in early developmental stages of rainbow trout (Onchorynchus mykiss) exposed to retene. J Toxicol Environ Health A 66:627–646CrossRefGoogle Scholar
  6. Carson J, Jenkins R, Wilson E, Howell W, Moore R (2008) Naturally occurring progesterone in loblolly pine (Pinus taeda L.): a major steroid precursor of environmental androgens. Environ Toxicol Chem 27:1273–1278CrossRefGoogle Scholar
  7. Chiang EFL, Yan YL, Guiguen Y, Postlethwait J, Chung BC (2001) Two cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain. Mol Biol Evol 18:542–550CrossRefGoogle Scholar
  8. Christianson-Heiska IL, Haavisto T, Paranko J, Bergelin E, Isomaa B (2008) Effects of wood extractives dehydroabietic acid and betulinol on reproductive physiology of zebrafish (Danio rerio)—a two-generation study. Aquat Toxicol 86:388–396CrossRefGoogle Scholar
  9. Costigan SL, Werner J, Ouellet JD, Hill LG, Law RD (2012) Expression profiling and gene ontology analysis in fathead minnow (Pimephales promelas) liver following exposure to pulp and paper mill effluents. Aquat Toxicol 122–123:44–55CrossRefGoogle Scholar
  10. Denslow ND, Kocerha J, Sepulveda MS, Gross T, Holm SE (2004) Gene expression fingerprints of largemouth bass (Micropterus salmoides) exposed to pulp and paper mill effluents. Mutat Res 552:19–34CrossRefGoogle Scholar
  11. Diniz MS, Peres I, Castro L, Freitas AC, Rocha-Santos TAP, Pereira R, Duarte AC (2010) Impact of a secondary treated bleached Kraft pulp mill effluent in both sexes of goldfish (Carassius auratus L.). J Environ Sci Health A 45:1858–1865CrossRefGoogle Scholar
  12. Diotel N, Le Page Y, Mouriec K, Tong SK, Pellegrini E, Vaillant C, Anglade I, Brion F, Pakdel F, Chung BC, Kah O (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 31:172–192CrossRefGoogle Scholar
  13. Doostdar H, Burke MD, Mayer RT (2000) Bioflavonoids: selective substrates and inhibitors for cytochrome P450 CYP1A and CYP1B1. Toxicology 144:31–38CrossRefGoogle Scholar
  14. Dranow DB, Tucker RP, Draper BW (2013) Germ cells are required to maintain a stable sexual phenotype in adult zebrafish. Dev Biol 376(1):43−50Google Scholar
  15. Ellis RJ, van den Heuvel MR, Stuthridge TR, Ling N, Dietrich DR (2004) Lack of estrogenic and endocrine disrupting effects of juvenile rainbow trout exposed to a New Zealand pulp and paper effluent. In: Borton DL, Hall TJ, Fisher RP, Thomas JF (eds) Pulp and paper mill effluent environmental fate and effects. DEStech Publication, Lancaster, pp 67–77Google Scholar
  16. Hawliczek A, Nota B, Cenjin P, Kamstra J, Pieterse B, Winter R, Winkems K, Hollert H, Segner H, Legler J (2012) Developmental toxicity and endocrine disrupting potency of 4-azapyrene, benzo[a]fluorine and retene in the zebrafish Danio rerio. Reprod Toxicol 33:213–223CrossRefGoogle Scholar
  17. Hewitt ML, Kovacs TG, Dube MG, MacLatchy DL, Martel PH, McMaster ME, Paice MG, Parrott JP, van den Heuvel MR, Van Der Kraak GJ (2008) Altered reproduction in fish exposed to pulp and paper mill effluents: roles of individual compounds and mill operating conditions. Environ Toxicol Chem 27:682–697CrossRefGoogle Scholar
  18. Hodson PV, Efler S, Wilson JY, El-Shaarawi A, Maj M, Williams TG (1996) Measuring the potency of pulp mill effluents for induction of hepatic mixed function oxygenase activity in fish. J Toxicol Environ Health 49:101–128Google Scholar
  19. Hyötyläinen T, Oikari A (1999) The toxicity and concentrations of PAHs in creosotecontaminated lake sediment. Chemosphere 38:1135−1144Google Scholar
  20. ISO 11348–1 (1998) Water quality-determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (Luminescence bacteria test)-Part 1: method using freshly prepared bacteria. International Organization for StandardizationGoogle Scholar
  21. ISO 21338 (2010) Water quality—kinetic determination of the inhibitory effects of sediment, other solids and coloured samples on the light emission of Vibrio fischeri (Kinetic luminescent bacteria test). International Organization for StandardizationGoogle Scholar
  22. Jenkins RL, Wilson EM, Angus RA, Howell WM, Kirk M (2003) Androstenedione and progesterone in the sediment of a river receiving paper mill effluent. Toxicol Sci 73:53–59CrossRefGoogle Scholar
  23. Karels AE, Soimasuo M, Lappivaara J, Leppänen H, Aaltonen T, Mellanen P, Oikari AOJ (1998) Effects of ECF-bleached kraft mill effluent on reproductive steroids and liver MFO activity in populations of perch and roach. Ecotoxicol 7:123–132CrossRefGoogle Scholar
  24. Karels A, Soimasuo M, Suutari R, Oikari A (2000) Monitoring the recovery of a polluted lake with biomarkers: responses of whitefish (Coregonus lavaretus L. s.I.) experimentally exposed to pulp and paper mill effluents. Boreal Environ Res 5:53–65Google Scholar
  25. Karels A, Markkula E, Oikari A (2001) Reproductive, biochemical, physiological, and population responses in perch (Perca fluviatilis L.) and roach (Rutilus rutilus L.) downstream of two elemental chlorine-free pulp and paper mills. Environ Toxicol Chem 22:1517–1527CrossRefGoogle Scholar
  26. Kishida M, Callard GV (2001) Distinct cytochrome p450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinol 142:740–750Google Scholar
  27. Kovacs T, Martel P, Ricci M, Michaud J, Voss R (2005) Further insights into the potential of pulp and paper mill effluents to affect fish reproduction. J Toxicol Environ Health A 68:1621–1641CrossRefGoogle Scholar
  28. Kurokawa H, Saito D, Nakamura S, Katoh-Fukui Y, Ohta K, Baba T, Morohashi K, Tanaka M (2007) Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci U S A 104:16958–16963CrossRefGoogle Scholar
  29. Lahdelma I, Oikari A (2005) Resin acids and retene in sediments adjacent to pulp and paper industries. J Soils Sediments 5:74–81CrossRefGoogle Scholar
  30. Lahdelma I, Oikari A (2006) Stratigraphy of wood-derived sterols in sediments historically contaminated by pulp and paper mill effluents. J Paleolimnol 35:323–334CrossRefGoogle Scholar
  31. Larsson DGJ, Hallman H, Forlin L (2000) More male fish embryos near a pulp mill. Environ Toxicol Chem 19:2911–2917CrossRefGoogle Scholar
  32. Lindström-Seppä P, Oikari, A (1990) Biotransformation activities of feral fish in waters receiving bleached pulp mill effluents. Environ Toxicol Chem 9:1415−1424Google Scholar
  33. Maack G, Segner H (2004) Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp Biochem Physiol C 139:47–55Google Scholar
  34. MacLatchy DL, Van Der Kraak GJ (1995) The phytoestrogen β-sitosterol alters the reproductive endocrine status of goldfish. Toxicol Appl Pharmacol 134:305–312CrossRefGoogle Scholar
  35. Mellanen P, Petänen T, Lehtimäki J, Mäkelä S, Bylund G, Holmbom B, Mannila E, Oikari A, Santti R (1996) Wood-derived estrogens: studies in vitro with breast cancer cell lines and in vivo in trout. Toxicol Appl Pharmacol 136:381–388CrossRefGoogle Scholar
  36. Mellanen P, Soimasuo M, Holmbom B, Oikari A, Santti R (1999) Expression of the vitellogenin gene in the liver of juvenile whitefish (Coregonus lavaretus L. s.I.) exposed to effluents from pulp and paper mills. Ecotoxicol Environ Saf 43:133–137CrossRefGoogle Scholar
  37. Meriläinen P, Lahdelma I, Oikari L, Hyötyläinen T, Oikari A (2006) Dissolution of resin acids, retene and wood sterols from contaminated lake sediments. Chemosphere 65:840–846CrossRefGoogle Scholar
  38. Mouriec K, Gueguen M-M, Manuel C, Percevault F, Thieulant M-L, Pakdel F, Kah O (2009) Androgens upregulate cyp19a1b (aromatase B) gene expression in the brain of zebrafish (Danio rerio) through estrogen receptors. Biol Reprod 80:889–896CrossRefGoogle Scholar
  39. Nakari T, Erkomaa K (2003) Effects of phytosterols on zebrafish reproduction in multigeneration tests. Environ Pollut 123:267–273CrossRefGoogle Scholar
  40. Nikkilä A, Kukkonen JVK, Oikari A (2001) Bioavailability of sediment-associated retene to oligochaete worm Lumbriculus variegatus. J Soils Sediments 1:137–145CrossRefGoogle Scholar
  41. Oakes KD, Trembley LA, Van Der Kraak GJ (2005) Short-term lab exposures of immature rainbow trout (Onchorynchus mykiss) to sulfite and kraft pulp-mill effluents: effects on oxidative stress and circulating sex steroids. Environ Toxicol Chem 24:1451–1461CrossRefGoogle Scholar
  42. Oikari A, Holmbom B (1996) Ecotoxicological effects of process changes implemented in a pulp and paper mill: a Nordic case study. In: Servos MR, Munkitrick KR, Carey JH, Van Der Kraak G (eds) Environmental fate and effects of pulp and paper mill effluents. St. Lucie Press, Florida, pp 613–625Google Scholar
  43. Oikari A, Nikinmaa M, Lindgren S, Lonn B (1985) Sublethal effects of simulated pulp mill effluents on the respiration and energy metabolism of rainbow trout (Salmo gairdneri). Ecotoxicol Environ Saf 9:378–384CrossRefGoogle Scholar
  44. Oikari A, Lahti M, Meriläinen P, Afanasyev S, Krasnov A (2010) Do historical sediments of pulp and paper industry contribute to the exposure of fish caged in receiving waters? J Environ Monit 12:1045–1054CrossRefGoogle Scholar
  45. Okuthe GE, Hanrahan S, Fabian BC (2014) Early gonad development in zebrafish (Danio rerio). Afr J Biotechnol 13:3433–3442CrossRefGoogle Scholar
  46. Organization for Economic Cooperation and Development (1992) Test no. 210: fish, early-life stage toxicity test, OECD guidelines for the testing of chemicals, Section 2, OECD Publishing, Paris, FranceGoogle Scholar
  47. Orlando EF, Davis WP, Guillette LJ Jr (2002) Aromatase activity in the ovary and brain of the eastern mosquitofish (Gambusia holbrooki) exposed to paper mill effluent. Environ Health Perspect 110(suppl 3):429–433CrossRefGoogle Scholar
  48. Örn S, Svenson A, Viktor T, Holbech H, Norrgren L (2006) Male-biased sex ratios and vitellogenin induction in zebrafish exposed to effluent water from a Swedish pulp mill. Arch Environ Contam Toxicol 51:445–451CrossRefGoogle Scholar
  49. Orrego R, Burgos A, Moraga-Cid G, Inzunza B, Gonzalez M, Valenzuela A, Barra R, Gavilan JE (2006) Effects of pulp and paper mill discharges on caged rainbow trout (Oncorhynchus mykiss): biomarker responses along a pollution gradient in the Biobio River, Chile. Environ Toxicol Chem 25:2280–2287CrossRefGoogle Scholar
  50. Orrego R, Guchardi H, Hernandez V, Krause R, Roti L, Armour J, Ganeshakumar M, Holdway D (2009) Pulp and paper mill effluent treatments have differential endocrine-disrupting effects on rainbow trout. Environ Toxicol Chem 28:181–188CrossRefGoogle Scholar
  51. Orrego R, Guchardi J, Krause R, Holdway D (2010a) Estrogenic and anti-estrogenic effects of wood extractives present in pulp and paper mill effluents on rainbow trout. Aquat Toxicol 99:160–167CrossRefGoogle Scholar
  52. Orrego R, McMaster M, Van Der Kraak G, Holdway D (2010b) Effects of pulp and paper mill effluent extractives on aromatase CYP19a gene expression and sex steroid levels in juvenile triploid rainbow trout. Aquat Toxicol 97:353–360CrossRefGoogle Scholar
  53. Orrego R, Pandelides Z, Guchardi J, Holdway D (2011) Effects of pulp and paper mill effluent extracts on liver anaerobic and aerobic metabolic enzymes in rainbow trout. Ecotoxicol Environ Saf 74:761–768CrossRefGoogle Scholar
  54. Pandelides Z, Guchardi J, Holdway D (2014) Dehydroabietic acid (DHAA) alters metabolic enzyme activity and the effects of 17β-estradiol in rainbow trout (Onchorynchus mykiss). Ecotoxicol Environ Saf 101:168–176CrossRefGoogle Scholar
  55. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45Google Scholar
  56. Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197:229–281CrossRefGoogle Scholar
  57. Ratia HM, Vehniäinen E-R, Rusanen AT, Oikari AOJ (2014) Recovery of historically contaminated watercourse polluted by the chemical wood industry: EROD activity in fish as biomarker. Soil Sediment Contam 23:211–225CrossRefGoogle Scholar
  58. Sahoo TP, Oikari A (2013) Use of early juvenile zebrafish Danio rerio for in-vivo assessment of endocrine modulation by xenoestrogens. J Environ Anal Toxicol 4:1–13Google Scholar
  59. Scholz S, Mayer I (2008) Molecular biomarkers of endocrine disruption in small model fish. Mol Cell Endocrinol 293:57–70CrossRefGoogle Scholar
  60. Sepúlveda MS, Gallagher EP, Wieser CM, Gross TS (2004) Reproductive and biochemical biomarkers in largemouth bass sampled downstream of a pulp and paper mill in Florida. Ecotoxicol Environ Saf 57:431–440CrossRefGoogle Scholar
  61. Sharpe RL, Woodhouse A, Moon TW, Trudeau VL, MacLatchy DL (2007) β-Sitosterol and 17β-estradiol alter gonadal steroidogenic acute regulatory protein (StAR) expression in goldfish, Carassius auratus. Gen Comp Endocrinol 151:34–41CrossRefGoogle Scholar
  62. Soimasuo MR, Karels AE, Lappivaara J, Oikari AOJ (1998a) Confirmation of in situ exposure of fish to secondary treated bleached-kraft mill effluent using a laboratory simulation. Environ Toxicol Chem 17:1371–1379CrossRefGoogle Scholar
  63. Soimasuo MR, Karels AE, Leppanen H, Oikari AOJ (1998b) Biomarker responses in whitefish (Coregonus lavaretus L. s.l.) experimentally exposed in a large lake receiving effluents from pulp and paper industry. Arch Environ Contam Toxicol 34:69–80CrossRefGoogle Scholar
  64. Takahashi H (1977) Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull Fac Fish Hokkaido Univ 28:57–65Google Scholar
  65. Teresaki M, Shirashi F, Fukazawa H, Makino M (2009) Development and validation of chemical and biological analyses to determine the antiestrogenic potency of resin acids in paper mill effluents. Environ Sci Technol 43:9300–9305CrossRefGoogle Scholar
  66. Tremblay L, Van Der Kraak GJ (1998) Use of a series of homologous in vitro and in vivo assays to evaluate the endocrine modulating actions of β-sitosterol in rainbow trout. Aquat Toxicol 43:149–162CrossRefGoogle Scholar
  67. Tremblay L, Van Der Kraak GJ (1999) Comparison between the effects of the phytosterol beta-sitosterol and pulp and paper mill effluents on sexually immature rainbow trout. Environ Toxicol Chem 18:329–336CrossRefGoogle Scholar
  68. Uchida D, Yamashita M, Kitano T, Iguchi T (2004) An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol A 137:11–20CrossRefGoogle Scholar
  69. van den Heuvel MR (2010) Recent progress in understanding the causes of endocrine disruption related to pulp and paper mill effluents. Water Qual Res J Can 45:137–144Google Scholar
  70. van den Heuvel MR, Ellis RJ (2002) Timing of exposure to a pulp and paper effluent influences the manifestation of reproductive effects in rainbow trout. Environ Toxicol Chem 21:2338–2347CrossRefGoogle Scholar
  71. Van Der Kraak GJ, Munkittrick KR, McMaster ME, Portt CB, Chang J (1992) Exposure to bleached kraft mill effluent disrupts the pituitary-gonadal axis of white sucker at multiple sites. Toxicol Appl Pharmacol 115:224–233CrossRefGoogle Scholar
  72. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Gen Biol 3:research0034−research0034.11Google Scholar
  73. Wang XG, Bartfai R, Sleptsova-Freidrich I, Orban L (2007) The timing and extent of ‘juvenile ovary’ phase are highly variable during zebrafish testis differentiation. J Fish Biol 70:33–44CrossRefGoogle Scholar
  74. Wang J, Shi X, Du Y, Zhou B (2011) Effects of xenoestrogens on the expression of vitellogenin (vtg) and cytochrome P450 aromatase (cyp19a and b) genes in zebrafish (Danio rerio) larvae. J Environ Sci Health A 46:960–967CrossRefGoogle Scholar
  75. Werner J, Ouellet JD, Cheng CS, Ju YJ, Law RD (2010) Pulp and paper mill effluents induce distinct gene expression changes linked to androgenic and estrogenic responses in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 29:430–439CrossRefGoogle Scholar
  76. Westerfield M (2007) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), 5th Edition. University of Oregon Press, EugeneGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Division of Environmental Science and TechnologyUniversity of JyväskyläJyväskyläFinland

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