Advertisement

BioNanoScience

, Volume 9, Issue 3, pp 758–764 | Cite as

Current Approaches to the Evaluation of Soil Genotoxicity

  • Airat R. KayumovEmail author
  • Dmitriy A. Solovyev
  • Denis E. Bobrov
  • Albert A. Rizvanov
Article
  • 38 Downloads

Abstract

Increasing human population, industrial activity, and intensive methods in agriculture have led to the release of various pollutants in soil, water, and air. While many organic compounds can be degraded by indigenous micro- and phytoflora, some pollutants are not degradable and accumulate in the environment. This requires regular monitoring of their presence for modeling and prognosis of their distribution and possible ecological risks. Conventionally all contaminants are classified by their effects on living organisms to the toxic and genotoxic ones. Toxic compounds lead to organism death, but genotoxic agents affect the genetic machinery of the cells causing mutations which can then be transmitted to offspring. The majority of pollutants have both toxic and genotoxic effects at high and low concentrations respectively. To date, various approaches to different fields of environmental toxicology for predicting the presence of toxic and mutagenic substances in soils are suggested. These tests can be classified by either biological system employed (bacteria, plants, or animals) or genetic endpoint detected. In this paper, we will review these experimental approaches, the level of their universality, advantages, and pitfalls when evaluating the mutagenic potential of contaminated soils.

Keywords

Genotoxicity Soil pollutants Environmental toxicology Biomarkers 

Notes

Funding Statement

This study was supported by the Russian Government Program of Competitive Development ofKazan Federal University. AK was supported by state assignment 1.12878.2018/12.1 of the Ministry of Science andHigher Education of Russian Federation.

Compliance with Ethical Standards

Conflict of Interest

None.

Informed Consent

None.

Research Involving Humans and Animals Statement

The article does not contain any study with human participants or animals performed by any of the authors.

References

  1. 1.
    Bhatti, S. S., Sambyal, V., & Nagpal, A. K. (2016). Heavy metals bioaccumulation in Berseem (Trifolium alexandrinum) cultivated in areas under intensive agriculture, Punjab, India. Springerplus, 5.Google Scholar
  2. 2.
    Tian, K., Huang, B., Xing, Z., & Hu, W. Y. (2017). Geochemical baseline establishment and ecological risk evaluation of heavy metals in greenhouse soils from Dongtai, China. Ecological Indicators, 72, 510–520.CrossRefGoogle Scholar
  3. 3.
    Bhatti, S. S., Sambyal, V., & Nagpal, A. K. (2018). Analysis of genotoxicity of agricultural soils and metal (Fe, Mn, and Zn) accumulation in crops. International Journal of Environmental Research, 12(4), 439–449.CrossRefGoogle Scholar
  4. 4.
    Gianfreda, L., & Rao, M. A. (2017). Soil microbial and enzymatic diversity as affected by the presence of xenobiotics. In Xenobiotics in the Soil Environment: Monitoring, Toxicity and Management (Vol. 49, pp. 153–169).CrossRefGoogle Scholar
  5. 5.
    Kues, U. (2015). Fungal enzymes for environmental management. Current Opinion in Biotechnology, 33, 268–278.CrossRefGoogle Scholar
  6. 6.
    Achuba, F. I., & Peretiemo-Clarke, B. O. (2008). Effect of spent engine oil on soil catalase and dehydrogenase activities. International Agrophysics, 22(1), 1–4.Google Scholar
  7. 7.
    Baran, S., Bielinska, J. E., & Oleszczuk, P. (2004). Enzymatic activity in an airfield soil polluted with polycyclic aromatic hydrocarbons. Geoderma, 118(3-4), 221–232.CrossRefGoogle Scholar
  8. 8.
    Mika, A., & Luthje, S. (2003). Properties of guaiacol peroxidase activities isolated from corn root plasma membranes. Plant Physiology, 132(3), 1489–1498.CrossRefGoogle Scholar
  9. 9.
    Siesko, M. M., Fleming, W. J., & Grossfeld, R. M. (1997). Stress protein synthesis and peroxidase activity in a submersed aquatic macrophyte exposed to cadmium. Environmental Toxicology and Chemistry, 16(8), 1755–1760.CrossRefGoogle Scholar
  10. 10.
    Pena, L. B., Tomaro, M. L., & Gallego, S. M. (2006). Effect of different metals on protease activity in sunflower cotyledons. Electronic Journal of Biotechnology, 9(3), 258–262.CrossRefGoogle Scholar
  11. 11.
    Palma, J. M., Sandalio, L. M., Corpas, F. J., Romero-Puertas, M. C., McCarthy, I., & del Rio, L. A. (2002). Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiology and Biochemistry, 40(6-8), 521–530.CrossRefGoogle Scholar
  12. 12.
    Trasar-Cepeda, C., Leiros, M. C., Seoane, S., & Gil-Sotres, F. (2000). Limitations of soil enzymes as indicators of soil pollution. Soil Biology & Biochemistry, 32(13), 1867–1875.CrossRefGoogle Scholar
  13. 13.
    Gil-Sotres, F., Trasar-Cepeda, C., Leiros, M. C., & Seoane, S. (2005). Different approaches to evaluating soil quality using biochemical properties. Soil Biology & Biochemistry, 37(5), 877–887.CrossRefGoogle Scholar
  14. 14.
    Fernandes, T. C. C., Mazzeo, D. E. C., & Marin-Morales, M. A. (2007). Mechanism of micronuclei formation in polyploidizated cells of Allium cepa exposed to trifluralin herbicide. Pesticide Biochemistry and Physiology, 88(3), 252–259.CrossRefGoogle Scholar
  15. 15.
    Turkoglu, S. (2007). Genotoxicity of five food preservatives tested on root tips of Allium cepa L. Mutation Research-Genetic Toxicology and Environmental Mutagenesis, 626(1-2), 4–14.CrossRefGoogle Scholar
  16. 16.
    SmakaKincl, V., Stegnar, P., Lovka, M., & Toman, M. J. (1996). The evaluation of waste, surface and ground water quality using the Allium test procedure. Mutation Research-Genetic Toxicology, 368(3-4), 171–179.CrossRefGoogle Scholar
  17. 17.
    Seth, C. S., Misra, V., Chauhan, L. K. S., & Singh, R. R. (2008). Genotoxicity of cadmium on root meristem cells of Allium cepa: cytogenetic and Comet assay approach. Ecotoxicology and Environmental Safety, 71(3), 711–716.CrossRefGoogle Scholar
  18. 18.
    Fiskesjo, G. (1985). The allium test as a standard in environmental monitoring. Hereditas, 102(1), 99–112.CrossRefGoogle Scholar
  19. 19.
    Albertini, R. J., Anderson, D., Douglas, G. R., Hagmar, L., Hemminki, K., Merlo, F., Natarajan, A. T., Norppa, H., Shuker, D. E. G., Tice, R., et al. (2000). IPCS guidelines for the monitoring of genotoxic effects of carcinogens in humans. Mutation Research-Reviews in Mutation Research, 463(2), 111–172.CrossRefGoogle Scholar
  20. 20.
    Bast, C. B., & Preston, R. J. (1986). Induction of chromosome-type aberrations by chemicals in G0-treated human-lymphocytes - a possible method of increasing the sensitivity of the lymphocyte assay. Environmental Mutagenesis, 8, 9–9.CrossRefGoogle Scholar
  21. 21.
    Rank, J., & Nielsen, M. H. (1993). A modified allium test as a tool in the screening of the genotoxicity of complex-mixtures. Hereditas, 118(1), 49–53.CrossRefGoogle Scholar
  22. 22.
    Leme, D. M., & Marin-Morales, M. A. (2009). Allium cepa test in environmental monitoring: a review on its application. Mutation Research-Reviews in Mutation Research, 682(1), 71–81.CrossRefGoogle Scholar
  23. 23.
    Araldi, R. P., de Melo, T. C., Mendes, T. B., de Sa, P. L., Nozima, B. H. N., Ito, E. T., de Carvalho, R. F., de Souza, E. B., & Stocco, R. D. (2015). Using the comet and micronucleus assays for genotoxicity studies: a review. Biomedicine & Pharmacotherapy, 72, 74–82.CrossRefGoogle Scholar
  24. 24.
    Leme, D. M., & Marin-Morales, M. A. (2008). Chromosome aberration and micronucleus frequencies in Allium cepa cells exposed to petroleum polluted water - a case study. Mutation Research-Genetic Toxicology and Environmental Mutagenesis, 650(1), 80–86.CrossRefGoogle Scholar
  25. 25.
    Ostling, O., & Johanson, K. J. (1984). Microelectrophoretic study of radiation-induced DNA damages in individual mammalian-cells. Biochemical and Biophysical Research Communications, 123(1), 291–298.CrossRefGoogle Scholar
  26. 26.
    Collins, A. R. (2004). The comet assay for DNA damage and repair - principles, applications, and limitations. Molecular Biotechnology, 26(3), 249–261.CrossRefGoogle Scholar
  27. 27.
    Augustyniak, M., Gladysz, M., & Dziewiecka, M. (2016). The Comet assay in insects status, prospects and benefits for science. Mutation Research-Reviews in Mutation Research, 767, 67–76.CrossRefGoogle Scholar
  28. 28.
    Cardoso, D. N., Silva, A. R. R., Cruz, A., Lourenco, J., Neves, J., Malheiro, C., Mendo, S., Soares, A., & Loureiro, S. (2017). The comet assay in Folsomia candida: a suitable approach to assess genotoxicity in collembolans. Environmental Toxicology and Chemistry, 36(9), 2514–2520.CrossRefGoogle Scholar
  29. 29.
    McKelvey-Martin, V. J., & McKenna, D. J. (2009). Development and applications of the Comet-FISH assay for the study of DNA damage and repair. In A. Dhawan & D. Anderson (Eds.), Comet assay in toxicology (Vol. 5, pp. 129–150).CrossRefGoogle Scholar
  30. 30.
    Spivak, G. (2010). The Comet-FISH assay for the analysis of DNA damage and repair. In J. M. Bridger & E. V. Volpi (Eds.), Fluorescence in situ hybridization (Vol. 659, pp. 129–145).CrossRefGoogle Scholar
  31. 31.
    Zainol, M., Stoute, J., Almeida, G. M., Rapp, A., Bowman, K. J., & Jones, G. D. D. (2009). Ecvag: Introducing a true internal standard for the Comet assay to minimize intra- and inter-experiment variability in measures of DNA damage and repair. Nucleic Acids Research, 37(22).Google Scholar
  32. 32.
    Collins, A. R., Oscoz, A. A., Brunborg, G., Gaivao, I., Giovannelli, L., Kruszewski, M., Smith, C. C., & Stetina, R. (2008). The comet assay: topical issues. Mutagenesis, 23(3), 143–151.CrossRefGoogle Scholar
  33. 33.
    van der Meer, J. R., & Belkin, S. (2010). Where microbiology meets microengineering: design and applications of reporter bacteria. Nature Reviews Microbiology, 8(7), 511–522.CrossRefGoogle Scholar
  34. 34.
    Baidamshina, D., Trizna, E., Akhatova, F., Holyavka, M., Rozhina, E., Fakhrullin, R., Bogachev, M., & Kayumov, A. (2016). The effect of ficin, a non-specific plant protease, on staphylococcal biofilms disruption. Febs Journal, 283, 289.Google Scholar
  35. 35.
    Elena, T., Diana, B., Marina, K., Irshad, S., Aigul, H., K, F., Elena, Z., Rais, H., & Airat, K. (2016). Soluble and immobilized papain and trypsin as destroyers of bacterial biofilms. Genes and Cells, 10(3), 106–112.Google Scholar
  36. 36.
    Holyavka, M. G., Kayumov, A. R., Baydamshina, D. R., Koroleva, V. A., Trizna, E. Y., Trushin, M. V., & Artyukhov, V. G. (2018). Efficient fructose production from plant extracts by immobilized inulinases from Kluyveromyces marxianus and Helianthus tuberosus. International Journal of Biological Macromolecules, 115, 829–834.CrossRefGoogle Scholar
  37. 37.
    Sharafutdinov, I. S., Trizna, E. Y., Baidamshina, D. R., Ryzhikova, M. N., Sibgatullina, R. R., Khabibrakhmanova, A. M., Latypova, L. Z., Kurbangalieva, A. R., Rozhina, E. V., Klinger-Strobel, M., et al. (2017). Antimicrobial effects of sulfonyl derivative of 2(5H)-furanone against planktonic and biofilm associated methicillin-resistant and -susceptible Staphylococcus aureus. Frontiers in Microbiology, 8.Google Scholar
  38. 38.
    Trizna, E. Y., Khakimullina, E. N., Latypova, L. Z., Kurbangalieva, A. R., Sharafutdinov, I. S., Evtyugin, V. G., Babynin, E. V., Bogachev, M. I., & Kayumov, A. R. (2015). Thio derivatives of 2(5H)-furanone as inhibitors against Bacillus subtilis biofilms. Acta Naturae, 7(2), 102–107.CrossRefGoogle Scholar
  39. 39.
    Trizna, E., Latypova, L., Kurbangalieva, A., Bogachev, M. I., & Kayumov, A. (2016). 2(5H)-Furanone derivatives as inhibitors of staphylococcal biofilms. Bionanoscience, 6(4), 423–426.CrossRefGoogle Scholar
  40. 40.
    Garipov, M. R., Pavelyev, R. S., Lisovskaya, S. A., Nikitina, E. V., Kayumov, A. R., Sabirova, A. E., Bondar, O. V., Malanyeva, A. G.,Aimaletdinov, A. M., Iksanova, A. G., Balakin, K. V. & Shtyrlin, Y. G. (2017). Fluconazole-pyridoxine bis-triazolium compounds with potent activity against pathogenic bacteria and fungi including their biofilm-embedded forms. Journal of Chemistry, 2017, p. 15. ArticleID 4761650Google Scholar
  41. 41.
    Sapozhnikov, S. V., Shtyrlin, N. V., Kayumov, A. R., Zamaldinova, A. E., Iksanova, A. G., Nikitina, E. V., Krylova, E. S., Grishaev, D. Y., Balakin, K. V., & Shtyrlin, Y. G. (2017). New quaternary ammonium pyridoxine derivatives: synthesis and antibacterial activity. Medicinal Chemistry Research, 26(12), 3188–3202.CrossRefGoogle Scholar
  42. 42.
    Shtyrlin, N. V., Sapozhnikov, S. V., Koshkin, S. A., Iksanova, A. G., Sabirov, A. H., Kayumov, A. R., Nureeva, A. A., Zeldi, M. I., & Shtyrlin, Y. G. (2015). Synthesis and antibacterial activity of novel quaternary ammonium pyridoxine derivatives. Medicinal Chemistry, 11(7), 656–665.CrossRefGoogle Scholar
  43. 43.
    Shtyrlin, N. V., Sapozhnikov, S. V., Galiullina, A. S., Kayumov, A. R., Bondar, O. V., Mirchink, E. P., Isakova, E. B., Firsov, A. A., Balakin, K. V., & Shtyrlin, Y. G. (2016). Synthesis and antibacterial activity of quaternary ammonium 4-deoxypyridoxine derivatives. Biomed Research International, 2016, pp. 8. ArticleID 3864193Google Scholar
  44. 44.
    Llagostera, M., Garrido, S., Guerrero, R., & Barbe, J. (1986). Induction of sos genes of Escherichia coli by chromium compounds. Environmental Mutagenesis, 8(4), 571–577.CrossRefGoogle Scholar
  45. 45.
    Ackerley, D. F., Barak, Y., Lynch, S. V., Curtin, J., & Matin, A. (2006). Effect of chromate stress on Escherichia coli K-12. Journal of Bacteriology, 188(9), 3371–3381.CrossRefGoogle Scholar
  46. 46.
    Mouchet, F., Gauthier, L., Mailhes, C., Jourdain, M. J., Ferrier, V., Triffault, G., & Devaux, A. (2006). Biomonitoring of the genotoxic potential of aqueous extracts of soils and bottom ash resulting from municipal solid waste incineration, using the comet and micronucleus tests on amphibian (Xenopus laevis) larvae and bacterial assays (Mutatox (R) and Ames tests). Science of the Total Environment, 355(1-3), 232–246.CrossRefGoogle Scholar
  47. 47.
    Ivask, A., Francois, M., Kahru, A., Dubourguier, H. C., Virta, M., & Douay, F. (2004). Recombinant luminescent bacterial sensors for the measurement of bioavailability of cadmium and lead in soils polluted by metal smelters. Chemosphere, 55(2), 147–156.CrossRefGoogle Scholar
  48. 48.
    Huang, W. E., Wang, H., Zheng, H. J., Huang, L. F., Singer, A. C., Thompson, I., & Whiteley, A. S. (2005). Chromosomally located gene fusions constructed in Acinetobacter sp. ADP1 for the detection of salicylate. Environmental Microbiology, 7(9), 1339–1348.CrossRefGoogle Scholar
  49. 49.
    Song, Y. Z., Jiang, B., Tian, S. C., Tang, H., Liu, Z. J., Li, C., Jia, J. L., Huang, W. E., Zhang, X., & Li, G. H. (2014). A whole-cell bioreporter approach for the genotoxicity assessment of bioavailability of toxic compounds in contaminated soil in China. Environmental Pollution, 195, 178–184.CrossRefGoogle Scholar
  50. 50.
    Jiang, B., Zhu, D., Song, Y. Z., Zhang, D. Y., Liu, Z. J., Zhang, X., Huang, W. E., & Li, G. H. (2015). Use of a whole-cell bioreporter, Acinetobacter baylyi, to estimate the genotoxicity and bioavailability of chromium(VI)-contaminated soils (vol 37, pg 343, 2015). Biotechnology Letters, 37(6), 1323–1323.CrossRefGoogle Scholar
  51. 51.
    Mortelmans, K., & Zeiger, E. (2000). The Ames Salmonella/microsome mutagenicity assay. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 455(1-2), 29–60.CrossRefGoogle Scholar
  52. 52.
    Levin, D. E., & Ames, B. N. (1984). Classifying mutagens as to their specificity in causing the 6 possible transitions and transversions - a simple analysis using the salmonella mutagenicity assay. Environmental Mutagenesis, 6(3), 388–388.Google Scholar
  53. 53.
    Lah, B., Vidic, T., Glasencnik, E., Cepeljnik, T., Gorjanc, G., & Marinsek-Logar, R. (2008). Genotoxicity evaluation of water soil leachates by Ames test, comet assay, and preliminary Tradescantia micronucleus assay. Environmental Monitoring and Assessment, 139(1-3), 107–118.CrossRefGoogle Scholar
  54. 54.
    Schrab, G. E., Brown, K. W., & Donnelly, K. C. (1993). Acute and genetic toxicity of municipal landfill leachate. Water Air and Soil Pollution, 69(1-2), 99–112.CrossRefGoogle Scholar
  55. 55.
    Wieczerzak, M., Namiesnik, J., & Kudlak, B. (2016). Bioassays as one of the Green Chemistry tools for assessing environmental quality: a review. Environment International, 94, 341–361.CrossRefGoogle Scholar
  56. 56.
    Oda, Y., Nakamura, S., Oki, I., Kato, T., & Shinagawa, H. (1985). Evaluation of the new system (umu-test) for the detection of environmental mutagens and carcinogens. Mutation Research, 147(5), 219–229.CrossRefGoogle Scholar
  57. 57.
    Wang, C. R., Tian, Y. A., Wang, X. R., Geng, J. J., Jiang, J. L., Yu, H. X., & Wang, C. (2010). Lead-contaminated soil induced oxidative stress, defense response and its indicative biomarkers in roots of Vicia faba seedlings. Ecotoxicology, 19(6), 1130–1139.CrossRefGoogle Scholar
  58. 58.
    Grant, W. F. (1999). Higher plant assays for the detection of chromosomal aberrations and gene mutations - a brief historical background on their use for screening and monitoring environmental chemicals. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 426(2), 107–112.MathSciNetCrossRefGoogle Scholar
  59. 59.
    Levan, A. (1938). The effect of colchicine on root mitoses in Allium. Hereditas, 24(4), 471–486.CrossRefGoogle Scholar
  60. 60.
    Grant, W. F. (1982). Chromosome aberration assays in Allium. Mutation Research, 99(3), 273–291.CrossRefGoogle Scholar
  61. 61.
    Steyn, M., Oberholster, P. J., Botha, A. M., Genthe, B., van den Heever-Kriek, P. E., & Weyers, C. (2019). Treated acid mine drainage and stream recovery: downstream impacts on benthic macroinvertebrate communities in relation to multispecies toxicity bioassays. Journal of Environmental Management, 235, 377–388.CrossRefGoogle Scholar
  62. 62.
    Young, B. J., Riera, N. I., Beily, M. E., Bres, P. A., Crespo, D. C., & Ronco, A. E. (2012). Toxicity of the effluent from an anaerobic bioreactor treating cereal residues on Lactuca sativa. Ecotoxicology and Environmental Safety, 76, 182–186.CrossRefGoogle Scholar
  63. 63.
    Dutka, B. (1989). In B. Dukta (Ed.), Short-term root elongation toxicity bioassay. Methods for toxicological analysis of waters, wastewaters and sediments (pp. 120–122). Burlington: National Water Research Institute (NWRI). Environment Canada.Google Scholar
  64. 64.
    Stolbova, V. V., Agapkina, G. I., Kotelnikova, A. D., Dogadova, A. V., & Abalymova, A. A. (2018). A short-term method for assessing the genotoxicity of soil as a solid-phase body based on the allium test. Moscow University Soil Science Bulletin, 73(5), 204–210.CrossRefGoogle Scholar
  65. 65.
    Iqbal, M. (2016). Vicia faba bioassay for environmental toxicity monitoring: a review. Chemosphere, 144, 785–802.CrossRefGoogle Scholar
  66. 66.
    Marcato-Romain, C. E., Guiresse, M., Cecchi, M., Cotelle, S., & Pinelli, E. (2009). New direct contact approach to evaluate soil genotoxicity using the Vicia faba micronucleus test. Chemosphere, 77(3), 345–350.CrossRefGoogle Scholar
  67. 67.
    Cotelle, S., Masfaraud, J. F., & Ferard, J. F. (1999). Assessment of the genotoxicity of contaminated soil with the Allium/Vicia-micronucleus and the Tradescantia-micronucleus assays. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 426(2), 167–171.CrossRefGoogle Scholar
  68. 68.
    Soil quality – assessment of genotoxic effects to higher plants – micronucleus test on Vicia faba. Editions AFNOR, 2004 Saint-Denis, 13pGoogle Scholar
  69. 69.
    White, P. A., & Claxton, L. D. (2004). Mutagens in contaminated soil: a review. Mutation Research-Reviews in Mutation Research, 567(2-3), 227–345.CrossRefGoogle Scholar
  70. 70.
    Ma, T. H., Xu, Z. D., Xu, C. G., McConnell, H., Rabago, E. V., Arreola, G. A., & Zhang, H. G. (1995). The improved allium vicia root-tip micronucleus assay for clastogenicity of environmental-pollutants. Mutation Research-Environmental Mutagenesis and Related Subjects, 334(2), 185–195.CrossRefGoogle Scholar
  71. 71.
    Steinkellner, H., Mun-Sik, K., Helma, C., Ecker, S., Ma, T. H., Horak, O., Kundi, M., & Knasmuller, S. (1998). Genotoxic effects of heavy metals: comparative investigation with plant bioassays. Environmental and Molecular Mutagenesis, 31(2), 183–191.CrossRefGoogle Scholar
  72. 72.
    Handy, R. D., Cornelis, G., Fernandes, T., Tsyusko, O., Decho, A., Sabo-Attwood, T., Metcalfe, C., Steevens, J. A., Klaine, S. J., Koelmans, A. A., et al. (2012). Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environmental Toxicology and Chemistry, 31(1), 15–31.CrossRefGoogle Scholar
  73. 73.
    Hracs, K., Savoly, Z., Seres, A., Kiss, L. V., Papp, I. Z., Kukovecz, A., Zaray, G., & Nagy, P. (2018). Toxicity and uptake of nanoparticulate and bulk ZnO in nematodes with different life strategies. Ecotoxicology, 27(8), 1058–1068.CrossRefGoogle Scholar
  74. 74.
    De Silva, P. M. C. S., & van Gestel, C. A. M. (2009). Comparative sensitivity of Eisenia andrei and Perionyx excavatus in earthworm avoidance tests using two soil types in the tropics. Chemosphere, 77(11), 1609–1613.CrossRefGoogle Scholar
  75. 75.
    Nahmani, J., & Lavelle, P. (2002). Effects of heavy metal pollution on soil macrofauna in a grassland of Northern France. European Journal of Soil Biology, 38(3-4), 297–300.CrossRefGoogle Scholar
  76. 76.
    Sturzenbaum, S. R., Kille, P., & Morgan, A. J. (1998). Identification of heavy metal induced changes in the expression patterns of the translationally controlled tumour protein (TCTP) in the earthworm Lumbricus rubellus. Biochimica Et Biophysica Acta-Gene Structure and Expression, 1398(3), 294–304.CrossRefGoogle Scholar
  77. 77.
    Chen, J. Q., Saleem, M., Wang, C. X., Liang, W. X., & Zhang, Q. M. (2018). Individual and combined effects of herbicide tribenuron-methyl and fungicide tebuconazole on soil earthworm Eisenia fetida. Scientific Reports, 8.Google Scholar
  78. 78.
    Cortet, J., Gomot-De Vauflery, A., Poinsot-Balaguer, N., Gomot, L., Texier, C., & Cluzeau, D. (1999). The use of invertebrate soil fauna in monitoring pollutant effects. European Journal of Soil Biology, 35(3), 115–134.CrossRefGoogle Scholar
  79. 79.
    Curieses, S. P., Saenz, M. E., Larramendy, M., & Di Marzio, W. (2016). Ecotoxicological evaluation of foundry sands and cosmetic sludges using new earthworm biomarkers. Ecotoxicology, 25(5), 914–923.CrossRefGoogle Scholar
  80. 80.
    Elyamine, A. M., Afzal, J., Rana, M. S., Imran, M., & Cai, M. M. (2018). Hu CX: Phenanthrene mitigates cadmium toxicity in earthworms Eisenia fetida (Epigeic Specie) and Aporrectodea caliginosa (Endogeic Specie) in Soil. International Journal of Environmental Research and Public Health, 15(11).Google Scholar
  81. 81.
    Van Hoesel, W., Tiefenbacher, A., Konig, N., Dorn, V. M., Hagenguth, J. F., Prah, U., Widhalm, T., Wiklicky, V., Koller, R., Bonkowski, M., et al. (2017). Single and combined effects of pesticide seed dressings and herbicides on earthworms, soil microorganisms, and litter decomposition. Frontiers in Plant Science, 8.Google Scholar
  82. 82.
    Xing, Y. S., Luo, J. H., Zhang, J. J., Li, B., Gong, X. Y., Liu, Z., & Liu, C. G. (2017). Effects of single and combined exposures to copper and benzotriazole on Eisenia fetida. Chemosphere, 186, 108–115.CrossRefGoogle Scholar
  83. 83.
    Xing, Y. S., Meng, X. S., Wang, L., Zhang, J. J., Wu, Z. J., Gong, X. Y., Wang, C. Y., & Sun, H. W. (2018). Effects of benzotriazole on copper accumulation and toxicity in earthworm (Eisenia fetida). Journal of Hazardous Materials, 351, 330–336.CrossRefGoogle Scholar
  84. 84.
    Garcia, E. M., da Silva, F. M. R., Tavella, R. A., Cruz, C. G., Baisch, P. R. M., & Muccillo-Baisch, A. L. (2017). Genotoxicity in the offspring of rats exposed to contaminated and acidified experimentally soils. Water Air and Soil Pollution, 228(7).Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Fundamental Medicine and BiologyKazan Federal UniversityKazanRussia
  2. 2.Biosphere and Technology LLCKazanRussia

Personalised recommendations