Abstract
Metals are always found in the environment as mixtures rather than as solitary elements. Only a limited number of studies have developed appropriate models that incorporate bioavailability to estimate the toxicity of heavy-metal mixtures. In the present study, we explored the applicability of two extended biotic ligand model (BLM) approaches—BLM-f mix and BLM-toxicity unit (TU)—to predict and interpret mixture toxicity with the assumption that interactions between metal ions obey the BLM theory. Exposure assays of single and mixed metals were performed with inoculums of an ammonia-oxidizing bacterium SD5 isolated from soil. Nitrification of the cultures was the end point used to quantify the toxic response. The results indicated that the developed BLM-f mix approach could well estimate the single toxicity of Cu2+ and Zn2+ as well as their binary mixture toxicity to nitrification with >90% of toxicity variation explained. Assuming that metal ions compete with each other for binding at a single biotic ligand, the BLM-f mix approach (root-mean-square error [RMSE] = 19.66, R 2 = 0.8879) showed better predictive power than the BLM-TU approach (RMSE = 31.12, R 2 = 0.6892). The present study supports the use of the accumulation of metal ions at the biotic ligands as predictor of toxicity of single metals and metal mixtures.
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References
Borgmann U, Norwood WP, Dixon DG (2008) Modelling bioaccumulation and toxicity of metal mixtures. Hum Ecol Risk Assess 14:266–289
Charles J, Crini G, Degiorgi F, Sancey B, Morin-Crini N, Badot PM (2014) Unexpected toxic interactions in the freshwater amphipod Gammarus pulex (L) exposed to binary copper and nickel mixtures. Environ Sci Pollut Res 21(2):1099–1111
Chen Z, Zhu L, Wilkinson KJ (2010) Validation of the biotic ligand model in metal mixtures: bioaccumulation of lead and copper. Environ Sci Technol 44:3580–3586
Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC (2001) Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ Toxicol Chem 20:2383–2396
Erickson RJ (2013) The biotic ligand model approach for addressing effects of exposure water chemistry on aquatic toxicity of metals: genesis and challenges. Environ Toxicol Chem 32:1212–1214
Guine V, Spadini L, Sarret G, Muris M, Delolme C, Gaudet JP et al (2006) Zinc sorption to three gram-negative bacteria: combined titration, modeling, and EXAFS study. Environ Sci Technol 40:1806–1813
Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman–Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719
Hatano A, Shoji R (2008) Toxicity of copper and cadmium in combinations to duckweed analyzed by the biotic ligand model. Environ Toxicol 23:372–378
He E, Van Gestel CAM (2015) Delineating the dynamic uptake and toxicity of Ni and Co mixtures in Enchytraeus crypticus using a WHAM-Ftox approaches. Chemosphere 139:216–222
Holm PE, Christensen TH, Tjell TC, McGrath SP (1995) Speciation of cadmium and zinc with application to soil solutions. J Environ Qual 24:183–190
Hu JL, Lin XG, Chu HY, Yin R, Zhang HY, Yuan XX et al (2005) Isolation of soil ammonia-oxidizing bacteria. Soil 37(5):569–571 (Chinese)
Iwasaki Y, Kamo M, Wataru N (2015) Testing an application of a biotic ligand model to predict acute toxicity of metal mixtures to rainbow trout. Environ Toxicol Chem 34(4):754–760
Jho EH, An J, Nam K (2011) Extended biotic ligand model for prediction of mixture toxicity of Cd and Pb using single metal toxicity data. Environ Toxicol Chem 30:1697–1703
Kamo M, Nagai T (2008) An application of the biotic ligand model to predict the toxic effects of metal mixtures. Environ Toxicol Chem 27:1479–1487
Khan FR, Keller W, Yan ND, Welsh PG, Wood CM, McGeer JC (2012) Application of biotic ligand and toxic unit modeling approaches to predict improvements in zooplankton species richness in smelter-damaged lakes near Sudbury, Ontario. Environ Sci Technol 46:1641–1649
Koops HP, Purkhold U, Pommerening-RoÈser A, Timmermann G, Wagner M (2003) In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackbrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York
Le TTY, Vijver MG, Hendriks Jan A, Peijnenburg WJGM (2013) Modeling toxicity of binary metal mixtures (Cu2+–Ag+, Cu) to lettuce, Lactuca sativa, with the biotic ligand model. Environ Toxicol Chem 32:137–143
Liu Y, Vijver MG, Peijnenburg WJGM (2014) Comparing three approaches in extending biotic ligand models to predict the toxicity of binary metal mixtures (Cu–Ni, Cu–Zn and Cu–Ag) to lettuce (Lactuca sativa L.). Chemosphere 112:282–288
Lock K, Janssen CR (2002) Mixture toxicity of zinc, cadmium, copper, and lead to the pot worm Enchytraeus albidus. Ecotoxicol Environ Saf 52:1–7
Mertens J, Degryse F, Springael D, Smolders E (2007) Zinc toxicity to nitrification in soil and soilless culture can be predicted with the same biotic ligand model. Environ Sci Technol 41(8):2992–2997
Meyer JS, Ranville JF, Pontash M, Gorsuch JW, Adams WJ (2015) Acute toxicity of binary and ternary mixtures of Cd, Cu, and Zn to Daphnia magna. Environ Toxicol Chem 34:799–808
Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192
Qiu H, Vijver MG, Peijnenburg WJGM (2011) Interactions of cadmium and zinc impact their toxicity to the earthworm Aporrectodea caliginosa. Environ Toxicol Chem 30:2084–2093
Qiu H, Vijver MG, He E, Liu Y, Wang P, Xia B et al (2015) Incorporating bioavailability into toxicity assessment of Cu–Ni, Cu–Cd, and Ni–Cd mixtures with the extended biotic ligand model and the WHAM-F tox approach. Environ Sci Pollut Res 22(23):19213–19223
Santore RC, Ryan AC (2015) Development and application of a multi-metal multi-biotic ligand model for assessing aquatic toxicity of metal mixtures. Environ Toxicol Chem 34:777–787
Slaveykova VI, Wilkinson KJ (2005) Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model. Environ Chem 2:9–24
Smolders E, Buekers J, Oliver I, McLaughlin MJ (2004) Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environ Toxicol Chem 23:2633–2640
Thakali S, Allen HE, Di Toro DM, Ponizovsky AA, Rooney CP, Zhao FJ et al (2006) A terrestrial biotic ligand model I: development and initial application to Cu and Ni toxicities o barley root elongation in soils. Environ Sci Technol 40(22):7085–7093
Vijver MG, Peijnenburg WJGM, De Snoo GR (2010) Toxicological mixture models are based on inadequate assumptions. Environ Sci Technol 44:4841–4842
Wilson DO (1977) Nitrification in three soils amended with zinc sulphate. Soil Biol Biochem 9:277–280
Acknowledgements
The study was supported by the National Natural Science Foundation of China (Grant No. 41671322), the Shandong Province Natural Fund (Grant No. 2015ZRB01615), and National Key Research and Development Project of China (Grant No. 2016YFD0800304).
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Liu, A., Li, J., Li, M. et al. Toxicity Assessment of Binary Metal Mixtures (Copper–Zinc) to Nitrification in Soilless Culture with the Extended Biotic Ligand Model. Arch Environ Contam Toxicol 72, 312–319 (2017). https://doi.org/10.1007/s00244-016-0346-9
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DOI: https://doi.org/10.1007/s00244-016-0346-9