Zinc's Role in Mitigating Copper Toxicity for Plants and Microorganisms in Industrially Contaminated Soils: A Review

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

This review focuses on the issue of metal antagonism in soils contaminated by multiple metals as a result of industrial emissions. Building upon previous findings in aquatic ecosystems, the potential of zinc to mitigate copper toxicity in more complex soil systems is explored. A range of studies investigating the role of zinc in reducing copper toxicity to plants and microorganisms in soils contaminated by copper mining in central Chile are examined. The mechanisms underlying metal interactions in soils, including the terrestrial biotic ligand model and the intensity/capacity/quantity concept, are thoroughly discussed. Furthermore, the review underscores the pressing need for future studies to enhance our understanding and develop effective strategies for mitigating copper toxicity in industrially contaminated soils.

About the authors

J. Santa-Cruz

Escuela de Ciencias Agrícolas y Veterinarias, Universidad Viña del Mar

Email: alexander.neaman@gmail.com
Viña del Mar, Chile

C. Yáñez

Instituto de Biología, Pontificia Universidad Católica de Valparaíso

Email: alexander.neaman@gmail.com
Valparaíso, Chile

A. Neaman

Departamento de Recursos Ambientales, Facultad de Ciencias Agronómicas, Universidad de Tarapacá

Email: alexander.neaman@gmail.com
Arica, Chile

E. A. Dovletyarova

Design and Sustainable Ecosystems, Peoples Friendship University of Russia (RUDN University)

Email: alexander.neaman@gmail.com
Moscow, Russia

T. A. Dubrovina

Design and Sustainable Ecosystems, Peoples Friendship University of Russia (RUDN University)

Email: alexander.neaman@gmail.com
Moscow, Russia

E. L. Vorobeichik

Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences

Email: alexander.neaman@gmail.com
Ekaterinburg, Russia

Yu. A. Krutyakov

Laboratory of Functional Materials for Agriculture, Department of Chemistry, Lomonosov Moscow State University; National Research Centre “Kurchatov Institute"

Author for correspondence.
Email: alexander.neaman@gmail.com
Moscow, Russia; Moscow, Russia

References

  1. Liu L.W., Li W., Song W.P., Guo M.X. Remediation techniques for heavy metal-contaminated soils: Principles and applicability // Science of the Total Environment. 2018. V. 633. P. 206–219. https://doi.org/10.1016/j.scitotenv.2018.03.161
  2. Wieser P.E., Jenner F.E. Chalcophile Elements: Systematics and Relevance // Encyclopedia of Geology (Second Edition). Eds. Alderton D., Elias S.A. 2021. P. 67–80.
  3. Preston S., Coad N., Townend J. et al. Biosensing the acute toxicity of metal interactions: Are they additive, synergistic, or antagonistic? // Environmental Toxicology and Chemistry. 2000. V. 19. № 3. P. 775–780. https://doi.org/10.1002/etc.5620190332
  4. Cedergreen N. Quantifying synergy: A systematic review of mixture toxicity studies within environmental toxicology // PloS One. 2014. V. 9. № 5. Article e96580. https://doi.org/10.1371/journal.pone.0096580
  5. Escher B.I., Stapleton H.M., Schymanski E.L. Tracking complex mixtures of chemicals in our changing environment // Science. 2020. V. 367. № 6476. P. 388–392. https://doi.org/10.1126/science.aay6636
  6. Bart S., Short S., Jager T. et al. How to analyse and account for interactions in mixture toxicity with toxicokinetic-toxicodynamic models // Science of the Total Environment. 2022. V. 843. Article 157048. https://doi.org/10.1016/j.scitotenv.2022.157048
  7. De Oliveira V.H., Tibbett M. Cd and Zn interactions and toxicity in ectomycorrhizal basidiomycetes in axenic culture // Peerj. 2018. V. 6. Article e4478. https://doi.org/10.7717/peerj.4478
  8. Duffus J.H. “Heavy metals” a meaningless term? (IUPAC Technical Report) // Pure and Applied Chemistry. 2002. V. 74. P. 793–807. https://doi.org/10.1351/pac200274050793
  9. Hodson M.E. Heavy metals - geochemical bogey men? // Environmental Pollution. 2004. V. 129. № 3. P. 341–343. https://doi.org/10.1016/j.envpol.2003.11.003
  10. Koptsik S.V., Koptsik G.N. Assessment of current risks of excessive heavy metal accumulation in soils based on the concept of critical loads: A review // Eurasian Soil Science. 2022. V. 55. № 5. P. 627–640. https://doi.org/10.1134/s1064229322050039
  11. Paquin P.R., Gorsuch J.W., Apte S. et al. The biotic ligand model: a historical overview // Comparative Biochemistry and Physiology C-Toxicology & Pharmacology. 2002. V. 133. № 1–2. P. 3–35. https://doi.org/10.1016/s1532-0456(02)00112-6
  12. Moiseenko T.I. Bioavailability and ecotoxicity of metals in aquatic systems: Critical contamination levels // Geochemistry International. 2019. V. 57. № 7. P. 737–750. https://doi.org/10.1134/s0016702919070085
  13. Bræk G.S., Jensen A., Mohus Å. Heavy metal tolerance of marine phytoplankton. III. Combined effects of copper and zinc ions on cultures of four common species // Journal of Experimental Marine Biology and Ecology. 1976. V. 25. № 1. P. 37–50. https://doi.org/https://doi.org/10.1016/0022-0981-(76)90074-5
  14. Dirilgen N., Inel Y. Effects of zinc and copper on growth and metal accumulation in duckweed, Leman-minor // Bulletin of Environmental Contamination and Toxicology. 1994. V. 53. № 3. P. 442–449. https://doi.org/10.1007/bf00197238
  15. Upadhyay R., Panda S.K. Zinc reduces copper toxicity induced oxidative stress by promoting antioxidant defense in freshly grown aquatic duckweed Spirodela polyrhiza L // Journal of Hazardous Materials. 2010. V. 175. № 1-3. P. 1081–1084. https://doi.org/10.1016/j.jhazmat.2009.10.016
  16. Otitoloju A.A. Evaluation of the joint-action toxicity of binary mixtures of heavy metals against the mangrove periwinkle Tympanotonus fuscatus var radula (L.) // Ecotoxicology and Environmental Safety. 2002. V. 53. № 3. P. 404–415. https://doi.org/https://doi.org/10.1016/S0147-6513-(02)00032-5
  17. Obiakor M.O., Ezeonyejiaku C.D. Copper-zinc coergisms and metal toxicity at predefined ratio concentrations: Predictions based on synergistic ratio model // Ecotoxicology and Environmental Safety. 2015. V. 117. P. 149–154. https://doi.org/10.1016/j.ecoenv.2015.03.035
  18. Le T.T.Y., Vijver M.G., Kinraide T.B. et al. Modelling metal-metal interactions and metal toxicity to lettuce Lactuca sativa following mixture exposure (Cu2+–Zn2+ and Cu2+–Ag+) // Environmental Pollution. 2013. V. 176. P. 185–192. https://doi.org/10.1016/j.envpol.2013.01.017
  19. Versieren L., Smets E., De Schamphelaere K. et al. Mixture toxicity of copper and zinc to barley at low level effects can be described by the Biotic Ligand Model // Plant and Soil. 2014. V. 381. № 1–2. P. 131–142. https://doi.org/10.1007/s11104-014-2117-6
  20. Liu Y., Vijver M.G., Peijnenburg W.J.G.M. 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. 2014. V. 112. P. 282–288. https://doi.org/10.1016/j.chemosphere.2014.04.077
  21. Thakali S., Allen H., Di Toro D. et al. A terrestrial biotic ligand model. 1. Development and application to Cu and Ni toxicities to barley root elongation in soils. // Environmental Science & Technology. 2006. V. 40. P. 7085–7093. https://doi.org/10.1021/es061171s
  22. Smolders E., Oorts K., van Sprang P. et al. Toxicity of trace metals in soil as affected by soil type and aging after contamination: Using calibrated bioavailability models to set ecological soil standards // Environmental Toxicology and Chemistry. 2009. V. 28. № 8. P. 1633–1642. https://doi.org/10.1897/08-592.1
  23. Neaman A., Selles I., Martínez C.E., Dovletyarova E.A. Analyzing soil metal toxicity: Spiked or field-contaminated soils? // Environmental Toxicology and Chemistry. 2020. V. 39. P. 513–514. https://doi.org/10.1002/etc.4654
  24. Santa-Cruz J., Vasenev I.I., Gaete H. et al. Metal ecotoxicity studies with spiked versus field-contaminated soils: Literature review, methodological shortcomings and research priorities // Russian Journal of Ecology. 2021. V. 52. № 6. P. 478–484. https://doi.org/10.1134/S1067413621060126
  25. Santa-Cruz J., Peñaloza P., Korneykova M.V., Neaman A. Thresholds of metal and metalloid toxicity in field-collected anthropogenically contaminated soils: A review // Geography, Environment, Sustainability. 2021. V. 14. № 2. P. 6–21. https://doi.org/10.24057/2071-9388-2021-023
  26. McBride M.B., Cai M.F. Copper and zinc aging in soils for a decade: Changes in metal extractability and phytotoxicity // Environmental Chemistry. 2016. V. 13. № 1. P. 160–167. https://doi.org/10.1071/en15057
  27. Ford R.G., Bertsch P.M., Farley K.J. Changes in transition and heavy metal partitioning during hydrous iron oxide aging // Environmental Science & Technology. 1997. V. 31. № 7. P. 2028–2033. https://doi.org/10.1021/es960824+
  28. Ávila G., Gaete H., Morales M., Neaman A. Reproducción de Eisenia fetida en suelos agrícolas de áreas mineras contaminadas por cobre y arsénico // Pesquisa Agropecuaria Brasileira. 2007. V. 42. № 3. P. 435–441. https://doi.org/10.1590/S0100-204X2007000300018
  29. Fischer E., Koszorus L. Sublethal effects, accumulation capacities and elimination rates of As, Hg and Se in the manure worm, Eisenia fetida (Oligochaeta, Lumbricidae) // Pedobiologia. 1992. V. 36. № 3. P. 172–178.
  30. Abbas M.S., Akmal M., Ullah S. et al. Effectiveness of zinc and gypsum application against cadmium toxicity and accumulation in wheat (Triticum aestivum L.) // Communications in Soil Science and Plant Analysis. 2017. V. 48. № 14. P. 1659–1668. https://doi.org/10.1080/00103624.2017.1373798
  31. Rehman M.Z.U., Rizwan M., Ali S. et al. Contrasting effects of organic and inorganic amendments on reducing lead toxicity in wheat // Bulletin of Environmental Contamination and Toxicology. 2017. V. 99. № 5. P. 642–647. https://doi.org/10.1007/s00128-017-2177-4
  32. Dubrovina T.A., Losev A.A., Karpukhin M.M. et al. Gypsum soil amendment in metal-polluted soils—an added environmental hazard // Chemosphere. 2021. V. 281. Article 130889. https://doi.org/10.1016/j.chemosphere.2021.130889
  33. Koptsik G.N., Koptsik S.V., Smirnova I.E. Alternative technologies for remediation of technogenic barrens in the Kola Subarctic // Eurasian Soil Science. 2016. V. 49. № 11. P. 1294–1309. https://doi.org/10.1134/s1064229316090088
  34. Neaman A. Metal phytoextraction from polluted soils: A utopian idea // Idesia (Chile). 2022. V. 40. № 4. P. 2–5. https://doi.org/10.4067/S0718-34292022000400002
  35. Neaman A. Soil metals // Idesia (Chile). 2022. V. 40. № 2. P. 2–6. https://doi.org/10.4067/S0718-34292022000200002
  36. Nahmani J., Hodson M.E., Black S. A review of studies performed to assess metal uptake by earthworms // Environmental Pollution. 2007. V. 145. № 2. P. 402–424. https://doi.org/10.1016/j.envpol.2006.04.009
  37. Verdejo J., Ginocchio R., Sauvé S. et al. Thresholds of copper phytotoxicity in field-collected agricultural soils exposed to copper mining activities in Chile // Ecotoxicology and Environmental Safety. 2015. V. 122. P. 171–177. https://doi.org/10.1016/j.ecoenv.2015.07.026
  38. Bustos V., Mondaca P., Sauvé S. et al. Thresholds of arsenic toxicity to Eisenia fetida in field-collected agricultural soils exposed to copper mining activities in Chile // Ecotoxicology and Environmental Safety 2015. V. 122. P. 448–454. https://doi.org/10.1016/j.ecoenv.2015.09.009
  39. Prudnikova E.V., Neaman A., Terekhova V.A. et al. Root elongation method for the quality assessment of metal-polluted soils: Whole soil or soil-water extract? // Journal of Soil Science and Plant Nutrition. 2020. V. 20. P. 2294–2303. https://doi.org/10.1007/s42729-020-00295-x
  40. Zhikharev A.P., Sahakyan L., Tepanosyan G. et al. Metal phytotoxicity thresholds in copper smelter-contaminated soils // Idesia (Chile). 2022. V. 40. № 3. P. 135–143. https://doi.org/10.4067/S0718-34292022000300135
  41. Artemyeva Z.S., Frid A.S., Titova V.I. The migration availability of potassium to plants on loamy soils // Agrokhimiya. 2019. V. 7. P. 16–26. https://doi.org/10.1134/s0002188119070032
  42. Il’in V.B. Heavy metals in the soil-crop system // Eurasian Soil Science. 2007. V. 40. № 9. P. 993–999. https://doi.org/10.1134/s1064229307090104
  43. Garcia J.M.V., Navarrete M.I.M., Saez J.A.L., Morencos I.D. Environmental impact of copper mining and metallurgy during the Bronze Age at Kargaly (Orenburg region, Russia) // Trabajos de Prehistoria. 2010. V. 67. № 2. P. 511–544. https://doi.org/10.3989/tp.2010.10054
  44. Dovletyarova E.A., Zhikharev A.P., Polyakov D.G. et al. Extremely high soil copper content, yet low phytotoxicity: A unique case of monometallic soil pollution at Kargaly, Russia // Environmental Toxicology and Chemistry. 2023. V. 42. № 3. P. 707–713. https://doi.org/10.1002/etc.5562
  45. Sauvé S., Cook N., Hendershot W.H., McBride M.B. Linking plant tissue concentrations and soil copper pools in urban contaminated soils // Environmental Pollution. 1996. V. 94. № 2. P. 153–157. https://doi.org/10.1016/S0269-7491(96)00081-4
  46. Kabata-Pendias A. Soil-plant transfer of trace elements – An environmental issue // Geoderma. 2004. V. 122. P. 143–149. https://doi.org/10.1016/j.geoderma.2004.01.004
  47. Lillo-Robles F., Tapia-Gatica J., Díaz-Siefer P. et al. Which soil Cu pool governs phytotoxicity in field-collected soils contaminated by copper smelting activities in central Chile? // Chemosphere. 2020. V. 242. Article 125 176. https://doi.org/10.1016/j.chemosphere.2019.125176
  48. Sauvé S., Dumestre A., McBride M., Hendershot W. Derivation of soil quality criteria using predicted chemical speciation of Pb2+ and Cu2+ // Environmental Toxicology and Chemistry. 1998. V. 17. № 8. P. 1481–1489. https://doi.org/10.1002/etc.5620170808
  49. Echevarria G., Morel J.L., Fardeau J.C., Leclerc-Cessac E. Assessment of phytoavailability of nickel in soils // Journal of Environmental Quality. 1998. V. 27. № 5. P. 1064–1070. https://doi.org/10.2134/jeq1998.00472425002700050011x
  50. Checkai R., Van Genderen E., Sousa J.P. et al. Deriving site-specific clean-up criteria to protect ecological receptors (plants and soil invertebrates) exposed to metal or metalloid soil contaminants via the direct contact exposure pathway // Integrated Environmental Assessment and Management. 2014. V. 10. № 3. P. 346-357. https://doi.org/10.1002/ieam.1528
  51. Spurgeon D.J., Ricketts H., Svendsen C. et al. Hierarchical responses of soil invertebrates (earthworms) to toxic metal stress // Environmental Science & Technology. 2005. V. 39. № 14. P. 5327–5334. https://doi.org/10.1021/es050033k
  52. Hassan M.J., Zhang G., Wu F. et al. Zinc alleviates growth inhibition and oxidative stress caused by cadmium in rice // Journal of Plant Nutrition and Soil Science. 2005. V. 168. P. 255–261. https://doi.org/10.1002/jpln.200420403
  53. Milone M.T., Sgherri C., Clijsters H., Navari-Izzo F. Antioxidative responses of wheat treated with realistic concentration of cadmium // Environmental and Experimental Botany. 2003. V. 50. № 3. P. 265–276. https://doi.org/10.1016/s0098-8472(03)00037-6
  54. Venkatachalam P., Jayaraj M., Manikandan R. et al. Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: A physiochemical analysis // Plant Physiology and Biochemistry. 2017. V. 110. P. 59–69. https://doi.org/10.1016/j.plaphy.2016.08.022
  55. Zhao A.Q., Tian X.H., Lu W.H. et al. Effect of zinc on cadmium toxicity in winter wheat // Journal of Plant Nutrition. 2011. V. 34. № 9–11. P. 1372–1385. https://doi.org/10.1080/01904167.2011.580879
  56. Cakmak I. Tansley review № 111 – Possible roles of zinc in protecting plant cells from damage by reactive oxygen species // New Phytologist. 2000. V. 146. № 2. P. 185–205. https://doi.org/10.1046/j.1469-8137.2000.00630.x
  57. Aravind P., Prasad M.N.V. Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: A free floating freshwater macrophyte // Plant Physiology and Biochemistry. 2003. V. 41. № 4. P. 391–397. https://doi.org/10.1016/s0981-9428(03)00035-4
  58. Tomasik P., Magadza C.M., Mhizha S. et al. Metal-metal interactions in biological systems. Part IV. Freshwater snail Bulinus globosus // Water Air and Soil Pollution. 1995. V. 83. № 1–2. P. 123–145. https://doi.org/10.1007/bf00482599
  59. Montvydiene D., Marciulioniene D. Assessment of toxic interaction of metals in binary mixtures using Lepidium sativum and Spirodela polyrrhiza // Polish Journal of Environmental Studies. 2007. V. 16. № 5. P. 777–783.
  60. Weast R. CRC Handbook of Chemistry and Physics. Cleveland: CRC Press, 1976.
  61. Kausar M.A., Chaudhry F.M., Rashid A. et al. Micronutrient availability to cereals from calcareous soils. 1. Comprative Zn and Cu deficiency and their mutual interaction in rice and wheat // Plant and Soil. 1976. V. 45. № 2. P. 397–410. https://doi.org/10.1007/bf00011702
  62. Stowhas T., Verdejo J., Yáñez C. et al. Zinc alleviates copper toxicity to symbiotic nitrogen fixation in agricultural soil affected by copper mining in central Chile // Chemosphere. 2018. V. 209 P. 960–963. https://doi.org/10.1016/j.chemosphere.2018.06.166
  63. McGrath S.P., Brookes P.C., Giller K.E. Effects of potentially toxic metals in soil derived from past applications of sewage sludge on nitrogen fixation by Trifolium repens L. // Soil Biology and Biochemistry. 1988. V. 20. № 4. P. 415–424. https://doi.org/https://doi.org/10.1016/0038-0717-(88)90052-1
  64. Broos K., Mertens J., Smolders E. Toxicity of heavy metals in soil assessed with various soil microbial and plant growth assays: A comparative study // Environmental Toxicology and Chemistry. 2005. V. 24. № 3. P. 634–640. https://doi.org/10.1897/04-036R.1
  65. Evdokimova G.A., Kalabin G.V., Mozgova N.P. Contents and toxicity of heavy metals in soils of the zone affected by aerial emissions from the Severonikel enterprise // Eurasian Soil Science. 2011. V. 44. № 2. P. 237–244. https://doi.org/10.1134/s1064229311020037
  66. Slukovskaya M.V., Kremenetskaya I.P., Ivanova L.A., Vasilieva T.N. Remediation in conditions of an operating copper-nickel plant: Results of perennial experiment // Non-ferrous Metals. 2017. V. 2. P. 20–26. https://doi.org/10.17580/nfm.2017.02.04
  67. Stuckey J.W., Neaman A., Verdejo J. et al. Zinc alleviates copper toxicity to lettuce and oat in copper contaminated soils // Journal of Soil Science and Plant Nutrition. 2021. V. 21. P. 1229–1235. https://doi.org/10.1007/s42729-021-00435-x
  68. Stuckey J.W., Mondaca P., Guzmán-Amado C. Impact of mining contamination source on copper phytotoxicity in agricultural soils from central Chile // AgroSur. 2021. V. 49. № 1. P. 21–27. https://doi.org/10.4206/agrosur.2021.v49n1-04
  69. Giller K.E., Witter E., McGrath S.P. Assessing risks of heavy metal toxicity in agricultural soils: Do microbes matter? // Human and Ecological Risk Assessment. 1999. V. 5. № 4. P. 683–689. https://doi.org/10.1080/10807039.1999.9657732
  70. Beyer W.N., Chaney R.L., Mulhern B.M. Heavy metal concentrations in earthworms from soil amended with sewage sludge // Journal of Environmental Quality. 1982. V. 11. № 3. P. 381–385. https://doi.org/10.2134/jeq1982.00472425001100030012x
  71. Kolbas A., Marchand L., Herzig R. et al. Phenotypic seedling responses of a metal-tolerant mutant line of sunflower growing on a Cu-contaminated soil series: Potential uses for biomonitoring of Cu exposure and phytoremediation // Plant and Soil 2014. V. 376. P. 377–397. https://doi.org/10.1007/s11104-013-1974-8
  72. Scott-Fordsmand J.J., Weeks J.M., Hopkin S.P. Importance of contamination history for understanding toxicity of copper to earthworm Eisenia fetida (Oligochaeta: Annelida), using neutral-red retention assay // Environmental Toxicology and Chemistry. 2000. V. 19. № 7. P. 1774–1780. https://doi.org/10.1002/etc.5620190710

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (89KB)
Indexing metadata
3.

Download (152KB)
Indexing metadata
4.

Download (101KB)
Indexing metadata
5.

Download (999KB)
Indexing metadata
6.

Download (214KB)
Indexing metadata

Copyright (c) 2023 Э.А. Довлетярова, Т.А. Дубровина, Е.Л. Воробейчик, Ю.А. Крутяков, Х. Санта-Круз, К. Яньез, А. Неаман

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies