Abstract
Background and purpose
The ubiquitous dissolved organic matter (DOM) is actually not inert as we always think, and the hormone-like effects of DOM have been reported. The objective of this study was to investigate the estrogenic effects of DOM and its impact on the activity of the natural estrogen 17β-estradiol (E2).
Materials and methods
DOM of three different sources, HA sodium salt, Suwannee River natural organic matter (NOM), and Nordic Reservoir NOM, were used. The estrogenic activity was detected by using the yeast estrogen screen (YES) assay. Estrogenic effects of DOM without and after solar irradiation were tested. Influences on the action of E2 by DOM were also investigated.
Results
No direct estrogenic effects of the DOM used were observed in the YES assay. However, the estrogenic activities after 24 h of irradiation increased to 0.0288, 0.0178, and 0.0195 μM of E2 equivalents for HA sodium salt, Suwannee River NOM, and Nordic Reservoir NOM, respectively. After incubation of DOM, the estrogenic activity of E2 was increased by low concentrations (8.33 and 83.3 μM) of DOM while decreased by higher concentrations (8.33 × 102 and 8.33 × 103 μM) of DOM.
Conclusions
Though direct estrogenic effects of DOM were not observed, increase in the estrogenic activity of DOM after irradiation was significant. DOM shows amphoteric influence on the natural estrogen E2, which depends on the concentration of DOM used. Because of its ubiquity, DOM may be of great ecological significance, playing an important role in regulating the reproduction of aquatic organisms.
Similar content being viewed by others
References
Akkanen J, Kukkonen JVK (2003) Measuring the bioavailability of two hydrophobic organic compounds in the presence of dissolved organic matter. Environ Toxicol Chem 22:518–524
Amine-Khodja A, Richard C, Lavedrine B, Guyot G, Trubetskaya O, Trubetskoj O (2006) Water-soluble fractions of composts for the photodegradation of organic pollutants in solar light. Environ Chem Lett 3:173–177
Bertilsson S, Tranvik LJ (1998) Photochemically produced carboxylic acids as substrates for freshwater bacterioplankton. Limnol Oceanogr 43:885–895
Bittner M, Janosek J, Hilscherova K, Giesy J, Holoubek I, Blaha L (2006) Activation of Ah receptor by pure humic acids. Environ Toxicol 21:338–342
Bittner M, Hilscherova K, Giesy JP (2007) Changes of AhR-mediated activity of humic substances after irradiation. Environ Int 33:812–816
Cory RM, McNeill K, Cotner JP, Amado A, Purcell JM, Marshall AG (2010) Singlet oxygen in the coupled photochemical and biochemical oxidation of dissolved organic matter. Environ Sci Technol 44:3683–3689
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
Elayan NM, Treleaven WD, Cook RL (2008) Monitoring the effect of three humic acids on a model membrane system using P-31 NMR. Environ Sci Technol 42:1531–1536
Frimmel FH (1994) Photochemical aspects related to humic substances. Environ Int 20:373–385
Gaido KW, Leonard LS, Lovell S, Gould CJ, Babai D, Portier CJ, McDonnell DP (1997) Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicol Appl Pharm 143:205–212
Haitzer M, Höss S, Traunspurger W, Steinberg C (1998) Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms. Chemosphere 37:1335–1362
Hessen DO, Faerovig PJ (2001) The photoprotective role of humus-DOC for Selenastrum and Daphnia. Plant Ecol 154:261–273
Höss S, Bergtold M, Haitzer M, Traunspurger W, Steinberg CEW (2001) Refractory dissolved organic matter can influence the reproduction of Caenorhabditis elegans (Nematoda). Freshwater Biol 46:1–10
Janošek J, Bittner M, Hilscherova K, Blaha L, Giesy JP, Holoubek I (2007) AhR-mediated and antiestrogenic activity of humic substances. Chemosphere 67:1096–1101
Kukkonen J, McCarthy JF, Oikari A (1990) Effects of XAD-8 fractions of dissolved organic carbon on the sorption and bioavailability of organic micropollutants. Arch Environ Contam Toxicol 19:551–557
Lee J, Cho J, Kim SH, Kim SD (2011) Influence of 17β-estradiol binding by dissolved organic matter isolated from wastewater effluent on estrogenic activity. Ecotox Environ Safe 74:1280–1287
Lutz I, Jie Z, Opitz R, Kloas W, Ying X, Menzel R, Steinberg CEW (2005) Environmental signals: Synthetic humic substances act as xeno-estrogen and affect the thyroid system of Xenopus laevis. Chemosphere 61:1183–1188
Ma M, Rao KF, Wang ZJ (2007) Occurrence of estrogenic effects in sewage and industrial wastewaters in Beijing. China Environ Pollut 147:331–336
Meinelt T, Schreckenbach K, Knopf K, Wienke A, Stuber A, Steinberg CEW (2004) Humic substances affect physiological condition and sex ratio of swordtail (Xiphophorus helleri Heckel). Aquat Sci 66:239–245
Menzel R, Sturzenbaum S, Barenwaldt A, Kulas J, Steinberg CEW (2005) Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ Sci Technol 39:8324–8332
Miller D, Wheals BB, Beresford N, Sumpter JP (2001) Estrogenic activity of phenolic additives determined by an in vitro yeast bioassay. Environ Health Persp 109:133–138
Muir DCG, Hobden BR, Servos MR (1994) Bioconcentration of pyrethroid insecticides and DTT by rainbow trout: uptake, depuration, and effect of dissolved organic carbon. Aquat Toxicol 29:230–240
Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002) Physiological effects of humic substances on higher plants. Soil Biol Biochem 34:1527–1536
Nishihara T, Nishikawa J, Kanayama T, Dakeyama F, Saito K, Imagawa M, Takatori S, Kitagawa Y, Hori S, Utsumi H (2000) Estrogenic activities of 517 chemicals by yeast two-hybrid assay. J Health Sci 46:282–298
Polewski K, Slawinska D, Slawinski J, Pawlak A (2005) The effect of UV and visible light radiation on natural humic acid EPR spectral and kinetic studies. Geoderma 126:291–299
Qiao P, Farrell AP (2002) Influence of dissolved humic acid on hydrophobic chemical uptake in juvenile rainbow trout. Comp Biochem Phys C 133:575–585
Rasmussen JB, Godbout L, Schallenberg M (1989) The humic content of lake water and its relationship to watershed and lake morphometry. Limnol Oceanogr 34:1336–1343
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
Steinberg CEW, Höss S, Brüggemann R (2002) Further evidence that humic substances have the potential to modulate the reproduction of the nematode Caenorhabditis elegans. Intern Rev Hydrobiol 87:121–133
Steinberg CEW, Kamara S, Prokhotskaya VY, Manusadzianas 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? Freshwater Biol 51:1189–1210
Thomas KV, Langford K, Petersen K, Smith AJ, Tollefsen KE (2009) Effect-directed identification of naphthenic acids as important in vitro xeno-estrogens and anti-androgens in north sea offshore produced water discharges. Environ Sci Technol 43:8066–8071
Timofeyev MA, Wiegand C, Burnison BK, Shatilina ZM, Pflugmacher S, Steinberg CEW (2004) Impact of natural organic matter (NOM) on freshwater amphipods. Sci Total Environ 319:115–121
Vigneault B, Percot A, Lafleur M, Campbell PGC (2000) Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Enviro Sci Technol 34:3907–3913
Wang JX, Wu WZ, Henkelmann B, You L, Kettrup A, Schramm KW (2003) Presence of estrogenic activity from emission of fossil fuel combustion as detected by a recombinant yeast bioassay. Atmos Environ 37:3225–3235
Yamamoto H, Liljestrand HM, Shimizu Y (2004) Effects of dissolved organic matter surrogates on the partitioning of 17β-estradiol and pnonylphenol between synthetic membrane vesicles and water. Environ Sci Technol 38:2351–2358
Acknowledgments
This work was supported by the Program for Changjiang Scholars and Innovative Research Team in University (IRT0536) and National Natural Science Foundation of China (20607019 and 40901153). We thank Naveedullah for language checking.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Henner Hollert
Rights and permissions
About this article
Cite this article
Chen, L., Shen, C., Tang, X. et al. Estrogenic effects of dissolved organic matter and its impact on the activity of 17β-estradiol. Environ Sci Pollut Res 19, 522–528 (2012). https://doi.org/10.1007/s11356-011-0590-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-011-0590-5