Abstract
The influence of dissolved organic carbon (DOC), in the form of Suwannee River fulvic acid (SRFA), on uranium (U) toxicity to the unicellular eukaryote, Euglena gracilis (Z strain), was investigated at pH 6. In a background medium without SRFA, exposure of E. gracilis to 57 μg L−1 U resulted in a 50% reduction in growth (IC50). The addition of 20 mg L−1 DOC (as SRFA), reduced U toxicity 4 to 5-fold (IC50 increased to 254 μg L−1 U). This reduction in toxicity was also evident at more sensitive effect levels with a 10% reduction in growth (IC10) occurring at 5 μg L−1 U in the background medium and at 17 μg L−1 U in the SRFA medium, respectively. This amelioration of toxicity with the addition of SRFA was linked to a decrease in the bioavailability of U, with geochemical speciation modelling predicting 84% of U would be complexed by SRFA. The decrease in bioavailability of U in the presence of SRFA was also evident from the 11–14 fold reduction in the cellular concentration of U compared to that of E. gracilis in the background medium. Stepwise multiple linear regression analyses indicated that UO2 2+ alone explained 51% of the variation in measured U toxicity to E. gracilis. Preliminary U exposures to E. gracilis in the presence of a reactive oxygen species probe, suggest exposure to ≥60 μg L−1 U may induce oxidative stress, but this endpoint was not considered to be a sensitive biological indicator.
Similar content being viewed by others
References
Antunes SC, Pereira R, Goncalves F (2007) Acute and chronic toxicity of effluent water from an abandoned uranium mine. Arch Environ Contam Toxicol 53:207–213
APHA, AWWA, WEF (2005) in: Eaton AD, Clesceri LS, Rice EW, Greenberg AE (eds) Standard methods for the examination of water and wastewater. American Public Health Association, American Water Works Assocation, Water Environment Federation, Washington DC
Barillet S, Adam C, Palluel O, Devaux A (2007) Bioaccumulation, oxidative stress, and neurotoxicity in Danio rerio exposed to different isotopic compositions of uranium. Environ Toxicol Chem 26:497–505
Barillet S, Larno V, Floriani M, Devaux A, Adam-Guillermin C (2010) Ultrastructural effects on gill, muscle, and gonadal tissues induced in zebrafish (Danio rerio) by a waterborne uranium exposure. Aquat Toxicol 100:295–302
Brown P, Haworth A, Sharland S, Tweed C (1991) HARPHRQ: an extended version of the geochemical code PHREEQE. NSS/R 188. UK Atomic Energy Authority, Oxford
Buet A, Barillet S, Camilleri V (2005) Changes in oxidative stress parameters in fish as response to direct uranium exposure. Radioprotection 40:S151–S155
Campbell PGC, Twiss MR, Wilkinson KJ (1997) Accumulation of natural organic matter on the surfaces of living cells: implications for the interaction of toxic solutes with aquatic biota. Can J Fish Aquat Sci 54:2543–2554
Danilov RA, Ekelund NGA (2001) Responses of photosynthetic efficiency, cell shape and motility in Euglena gracilis (Euglenophyceae) to short-term exposure to heavy metals and pentachlorophenol. Water Air Soil Pollut 132:61–73
dos Santos Ferreira V, Roccetta I, Conforti V, Bench S, Feldman R, Levin M (2007) Gene expression patterns in Euglena gracilis: insights into the cellular response to environmental stress. Gene 389:136–145
Einicker-Lamas M, Soares MJ, Soares MS, Oliveira MM (1996) Effects of cadmium on Euglena gracilis membrane lipids. Braz J Med Biol Res 29:941–948
Einicker-Lamas M, Meziana GA, Fernandesa TB, Silva FLS, Guerra F, Miranda K, Attias M, Oliveira MM (2002) Euglena gracilis as a model for the study of Cu2+ and Zn2+ toxicity and accumulation in eukaryotic cells. Environ Pollut 120:779–786
Franklin NM, Stauber JL, Markich SJ, Lim RP (2000) pH-dependent toxicity of copper and uranium to a tropical freshwater alga (Chlorella sp.). Aquat Toxicol 48:275–289
Gajdosova J, Reichrtova E (1996) Different growth response of Euglena gracilis to Hg, Cd, Cr and Ni compounds. Anal Bioanal Chem 354:641–642
Gianguzza A, Pettignano A, Sammartano S (2005) Interaction of the dioxouranium(VI) ion with aspartate and glutamate in NaCl(aq) at different ionic strengths. J Chem Eng Data 50:1576–1581
Glaus M, Hummel W, Van Loon L (2000) Trace metal-humate interactions. I. Experimental determination of conditional stability constants. Appl Geochem 15:953–973
Good NE, Winget GD, Winter W, Izawa S, Singh RMM (1966) Hydrogen ion buffers for biological research. Biochemistry 5:467–477
Hempel SL, Buettner GR, O’Malley YQ, Wessels DA, Flaherty DM (1999) Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 29,79-dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-29,79- dichlorodihydrofluorescein diacetate and dihydrorhodamine 123. Free Radic Biol Med 27:146–159
Hogan AC, van Dam RA, Markich SJ, Camilleri C (2005) Chronic toxicity of uranium to a tropical green alga (Chlorella sp.) in natural waters and the influence of dissolved organic carbon. Aquat Toxicol 75:343–353
Hynes TP, Schmidt RM, Meadley T, Thompson NA (1987) The impact of effluents from a uranium mine and mill complex in Northern Saskatchewan on contaminant concentrations in receiving waters and sediments. Water Pollut Res J Can 22:559–569
International Atomic Energy Agency (2008) Energy, electricity and nuclear power estimates for the period to 2030. Reference Data Series No. 1. Vienna
International Humic Substances Society (2008) Source materials for IHSS samples. http://www.humicsubstances.org/sources.html. Accessed Jan 2011
Invitrogen (2006) Reactive oxygen species (ROS) detection reagents. http://probes.invitrogen.com/media/pis/mp36103.pdf. Accessed Jan 2011
Invitrogen (2011) CM-H2DCFDA (general oxidative stress indicator). http://products.invitrogen.com/ivgn/product/C6827. Accessed 7 Apr 2011
Kaddissi SA, Legeay A, Gonzalez P, Floriani M, Camilleri V, Gilbin R, Simon O (2011) Effects of uranium uptake on transcriptional responses, histological structures and survival rate of the crayfish Procambarusclarkii. Ecotoxicol Environ Safe 74:1800–1807
Koren LE, Hutner SH (1967) High-yield media for photosynthesizing Euglena gracilis Z. J Protozool 14 (suppl):17
Lacky J (1968) Ecology of Euglena. In: Beutow DE (ed) The biology of Euglena, vol I. Academic Press, New York, pp 27–44
Landa ER, Gray JR (1995) US geological survey research on the environmental fate of uranium mining and milling wastes. Environ Geol 26:19–31
Malcolm RL (1985) Geochemistry of stream fulvic and humic substances. In: Aiken GR, McKnight DM, Wershaw RL (eds) Humic substances in soil, sediment, and water. Wiley, New York, pp 181–209
Markich SJ, Brown PL (1999) Thermochemical data (log K) for environmentally-relevant elements. Commonweath of Australia, Sydney
Markich SJ, Brown PL, Jeffree RA, Lim RP (2000) Valve movement responses of Velesunio angasi (Bivalvia: Hyriidae) to manganese and uranium: an exception to the free ion activity model. Aquat Toxicol 51:155–175
Mathews T, Beaugelin-Seiller K, Garnier-Laplace J, Gilbin R, Adam C, Della-Vedova C (2009) A probabilistic assessment of the chemical and radiological risks of chronic exposure to uranium in freshwater ecosystems. Environ Sci Technol 43:6684–6690
Matsuo AYO, Playle RC, Val AL, Wood CM (2004) Physiological action of dissolved organic matter in rainbow trout in the presence and absence of copper: sodium uptake kinetics and unidirectional flux rates in hard and softwater. Aquat Toxicol 70:63–81
Meybeck M (2003) Global occurrence of major elements in rivers. In: Drever JI (ed) Treatise on geochemistry, surface and groundwater, weathering and soils. Elsevier, London, pp 207–223
Mladenov N, McKnight DM, Wolski P, Ramberg L (2005) Effects of annual flooding on dissolved organic carbon dynamics within a pristine wetland, the Okavango Delta, Botswana. Wetlands 25:622–638
Navarro L, Torres-Marquez ME, Gonzalez-Moreno S, Devars S, Hernandez R, Moreno-Sanchez R (1997) Comparison of physiological changes in Euglena gracilis during exposure to heavy metals of heterotrophic and autotrophic cells. Comp Biochem Physiol C 116:265–272
Nechay BR, Thompson JD, Palmer Saunders J (1980) Inhibition by uranyl nitrate of adenosine triphosphatases derived from animal and human tissues. Toxicol Appl Pharm 53:410–419
Ohta M, Okazaki S, Hiramatsu M, Suzuki T (2001) Comparative studies on the cellular response to chemical loading in unicellular eukaryote, Euglena gracilis, strains Z and SMZ. Nutr Res 18:83–89
Overbaugh JM (1985) Initial observations on the role of glutathione peroxidases in euglena. Free Radic Biol Med 1:187–193
Parent L, Twiss M, Campbell P (1996) Influences of natural dissolved organic matter on the interaction of aluminum with the microalga Chlorella: a test of the free-ion model of trace metal toxicity. Environ Sci Technol 30:1713–1720
Periyakaruppan A, Kumar F, Sarkar S, Sharma CS, Ramesh GT (2007) Uranium induces oxidative stress in lung epithelial cells. Arch Toxicol 81:389–395
Pyle GG, Swanson SM, Lehmkuhl DM (2002) Toxicity of uranium mine receiving waters to early life stage fathead minnows (Pimephales promelas) in the laboratory. Environ Pollut 116:243–255
Ribera D, Labrot F, Tisnerat G, Narbonne JF (1996) Uranium in the environment: occurrence, transfer and biological effects. Rev Environ Contam Toxicol 146:53–89
Semaan M, Holdway DA, van Dam RA (2001) Comparative sensitivity of three populations of the cladoceran Moinodaphnia macleayi to acute and chronic uranium exposure. Environ Toxicol 16:365–376
Trenfield MA, Ng JC, Noller BN, Markich SJ, van Dam RA (2011a) Dissolved organic carbon reduces uranium bioavailability and toxicity. 2. Uranium[VI] speciation and toxicity to three tropical freshwater organisms. Environ Sci Technol 45:3082–3089
Trenfield MA, McDonald S, Kovacs K, Lesher E, Pringle JM, Markich SJ, Ng JC, Noller BN, Brown PL, van Dam RA (2011b) Dissolved organic carbon reduces uranium bioavailability and toxicity. 1. Characterization of an aquatic fulvic acid and its complexation with uranium[VI]. Environ Sci Technol 45:3075–3081
Watanabe M, Suzuki T (2001) Cadmium-induced abnormality in strains of Euglena gracilis: morphological alteration and its prevention by zinc and cyanocobalamin. Comp Biochem Phys C 130:29–39
Watanabe M, Suzuki T (2002) Involvement of reactive oxygen stress in cadmium-induced cellular damage in Euglena gracilis. Comp Biochem Physiol C 131:491–500
Yazzie M, Gamble SL, Civitello ER, Stearns DM (2003) Uranyl acetate causes DNA single strand breaks in vitro in the presence of ascorbate (Vitamin C). Chem Res Toxicol 16:524–530
Zeman FA, Gilbin R, Alonzo F, Lecomte-Pradines C, Garnier-Laplace J, Aliaume C (2008) Effects of waterborne uranium on survival, growth, reproduction and physiological processes of the freshwater cladoceran Daphnia magna. Aquat Toxicol 86:370–378
Acknowledgments
The authors would like to thank Professor Tetsuya Suzuki, Professor Mari Ohta and Dr. Masumi Watanabe at the Graduate School for Creation of New Photonics Industry, Japan for providing the E. gracilis Z strain and culturing advice and Dr. David Jones at eriss for providing comments on the manuscript. This project was funded by an ARC-Linkage grant (LP 0562507). EnTox is a partnership between Queensland Health and The University of Queensland.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Trenfield, M.A., Ng, J.C., Noller, B. et al. Dissolved organic carbon reduces uranium toxicity to the unicellular eukaryote Euglena gracilis . Ecotoxicology 21, 1013–1023 (2012). https://doi.org/10.1007/s10646-012-0855-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-012-0855-x