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Biochar reduces the toxicity of silver to barley (Hordeum vulgare) and springtails (Folsomia candida) in a natural soil

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Abstract

The use of biochar in soil remediation is a promising method to deal with metal contamination. In the present study, the influence of biochar amendment on the toxicity of silver (as AgNO3) to terrestrial organisms was assessed. For this, toxicity tests were conducted with terrestrial plant barley (Hordeum vulgare) and invertebrate springtails (Folsomia candida) in the standard natural Lufa soil amended or not with a wood-derived biochar at 5% (w/w). Biochar addition increased root length and mass in barley, compared to unamended soil. However, the effects of Ag on barley growth were masked by a great variation among replicates in biochar-amended soil. Photosynthetic pigment contents (total chlorophyll and carotenoids) were lower in plants exposed to Ag in Lufa soil, but not in biochar-amended soil. Moreover, Ag drastically decreased dehydrogenase activity in Lufa soil. For springtails, the addition of biochar clearly decreased the toxicity of Ag. The LC50 was 320 mg Ag/kg in Lufa soil, while no mortality was observed up to 500 mg Ag/kg in biochar-amended soil. The EC50 for effects on reproduction was significantly higher in biochar-amended soil compared to unamended Lufa soil (315 and 215 mg Ag/kg, respectively). The wood-derived biochar used in this study has shown a potential for remediation of contaminated soils, as a decrease in Ag toxicity was observed in most endpoints analysed in barley and springtails.

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All data generated or analysed during this study are included in this published article [and its supplementary information files].

References

  • Ameloot N, De Neve S, Jegajeevagan K, Yildiz G, Buchan D, Funkuin YN, Prins W, Bouckaert L, Sleutel S (2013) Short-term CO2 and N2O emissions and microbial properties of biochar amended sandy loam soils. Soil Biol Biochem 57:401–410

    Article  CAS  Google Scholar 

  • Ardestani MM, van Gestel CAM (2013) Dynamic bioavailability of copper in soil estimated by uptake and elimination kinetics in the springtail Folsomia candida. Ecotoxicology 22:308–318

    Article  CAS  Google Scholar 

  • Bogusz A, Nowak K, Stefaniuk M, Dobrowolski R, Oleszczuk P (2017) Synthesis of biochar from residues after biogas production with respect to cadmium and nickel removal from wastewater. J Environ Manage 201:268–276

    Article  CAS  Google Scholar 

  • Chaperon S, Sauvé S (2008) Toxicity interactions of cadmium, copper, and lead on soil urease and dehydrogenase activity in relation to chemical speciation. Ecotox Environ Safe 70:1–9

    Article  CAS  Google Scholar 

  • Conti FD, Visioli G, Malcevschi A, Menta C (2018) Safety assessment of gasification biochars using Folsomia candida (Collembola) ecotoxicological bioassays. Environ Sci Pollut Res 25:6668–6679

    Article  CAS  Google Scholar 

  • Coskun D, Britto DT, Jean YK, Schulze LM, Becker A, Kronzucker HJ (2012) Silver ions disrupt K+ homeostasis and cellular integrity in intact barley (Hordeum vulgare L.) roots. J Exp Bot 63:151–162

    Article  CAS  Google Scholar 

  • Courtois P, Rorat A, Lemiere S, Guyoneaud R, Attard E, Levard C, Vandenbulcke F (2019) Ecotoxicology of silver nanoparticles and their derivatives introduced in soil with or without sewage sludge: A review of effects on microorganisms, plants and animals. Environ Pollut 253:578–598

    Article  CAS  Google Scholar 

  • Dhaliwal SS, Singh J, Taneja PK, Mandal A (2020) Remediation techniques for removal of heavy metals from the soil contaminated through different sources: a review. Environ Sci Pollut Res 27:1319–1333

    Article  Google Scholar 

  • Fayez KA, El-Deeb BA, Mostafa NY (2017) Toxicity of biosynthetic silver nanoparticles on the growth, cell ultrastructure and physiological activities of barley plant. Acta Physiol Plant 39:1–13

    Article  CAS  Google Scholar 

  • Fountain MT, Hopkin SP (2005) Folsomia candida (Collembola): a “standard” soil arthropod. Annu Rev Entomol 50:201–222

    Article  CAS  Google Scholar 

  • van Gestel CAM (2008) Physico-chemical and biological parameters determine metal bioavailability in soils. Sci Total Environ 406:385–395

    Article  CAS  Google Scholar 

  • Gomes SIL, Scott-Fordsmand JJ, Amorim MJB (2015) Cellular energy allocation to assess the impact of nanomaterials on soil invertebrates (Enchytraeids): the effect of Cu and Ag. Int J Environ Res Public Health 12:6858–6878

    Article  CAS  Google Scholar 

  • González Linares M, Jia Y, Sunahara GI, Whalen JK (2020) Barley (Hordeum vulgare) seedling growth declines with increasing exposure to silver nanoparticles in biosolid-amended soils. Can J Soil Sci 100:189–197

    Article  CAS  Google Scholar 

  • Hopkins D, Hawboldt K (2020) Biochar for the removal of metals from solution: a review of lignocellulosic and novel marine feedstocks. J Environ Chem Eng 8:103975

    Article  CAS  Google Scholar 

  • Hou D, O’Connor D, Igalavithana AD, Alessi DS, Luo J, Tsang DCW, Sparks DL, Yamauchi Y, Rinklebe J, Ok YS (2020) Metal contamination and bioremediation of agricultural soils for food safety and sustainability. Nat Rev Earth Environ 1:366–381

    Article  Google Scholar 

  • ISO (1995) Soil Quality: Determination of the Effect of Pollutants on Soil Flora, Part 2: Effects of Chemicals on the Emergence and Growth of Higher Plants. Switzerland, Geneva

    Google Scholar 

  • ISO (2002) Soil quality: Determination of dehydrogenase activity in soils, part 1: method using triphenyltetrazolium chloride (TTC). International Organization for Standardization, Geneve, Switzerland

  • ISO (2005) Soil Quality: Determination of pH. ISO 10390. International Organization for Standardization, Geneve

  • Kończak M, Oleszczuk P, Różyło K (2019) Application of different carrying gases and ratio between sewage sludge and willow for engineered (smart) biochar production. J CO2 Utilization 29:20–28

  • Kończak M, Oleszczuk P (2020) Co-pyrolysis of sewage sludge and biomass in carbon dioxide as a carrier gas affects the total and leachable metals in biochars. J Hazard Mater 400:123144

    Article  CAS  Google Scholar 

  • Kończak M, Pan B, Ok YS, Oleszczuk P (2020) Carbon dioxide as a carrier gas and mixed feedstock pyrolysis decreased toxicity of sewage sludge biochar. Sci Total Environ 723:137796

    Article  CAS  Google Scholar 

  • Langdon KA, McLaughlin MJ, Kirby JK, Merrington G (2015) Influence of soil properties and soil leaching on the toxicity of ionic silver to plants. Environ Toxicol and Chem 34:2503–2512

    Article  CAS  Google Scholar 

  • Lehmann J, Gaunt J, Rondon M (2006) Bio-char sequestration in terrestrial ecosystems–a review. Mitig Adapt Strat Gl Change 11:403–427

    Article  Google Scholar 

  • Liang L, Xi F, Tan W, Meng X, Hu B, Wang X (2021) Review of organic and inorganic pollutants removal by biochar and biochar-based composites. Biochar 3:255–281

    Article  CAS  Google Scholar 

  • Lock K, Van Eeckhout H, De Schamphelaere KAC, Criel P, Janssen CR (2007) Development of a biotic ligand model (BLM) predicting nickel toxicity to barley (Hordeum vulgare). Chemosphere 66:1346–1352

    Article  CAS  Google Scholar 

  • Maria VL, Ribeiro MJ, Guilherme S, Soares AMVM, Scott-Fordsmand JJ, Amorim MJB (2018) Silver (nano) materials cause genotoxicity in Enchytraeus crypticus, as determined by the comet assay. Environ Toxicol Chem 37:184–191

    Article  CAS  Google Scholar 

  • Mendes LA, Maria VL, Scott-Fordsmand JJ, Amorim MJB (2015) Ag nanoparticles (Ag NM300K) in the terrestrial environment: Effects at population and cellular level in Folsomia candida (Collembola). Int J Environ Res Public Health 12:12530–12542

    Article  CAS  Google Scholar 

  • Mo F, Li H, Li Y, Cui W, Wang M, Li Z, Chai R, Wang H (2020) Toxicity of Ag+ on microstructure, biochemical activities and genic material of Trifolium pratense L. seedlings with special reference to phytoremediation. Ecotox Environ Safe 195:110499

    Article  CAS  Google Scholar 

  • Novo M, Lahive E, Díez-Ortiz M, Matzke M, Morgan AJ, Spurgeon DJ, Svendsen C, Kille P (2015) Different routes, same pathways: Molecular mechanisms under silver ion and nanoparticle exposures in the soil sentinel Eisenia fetida. Environ Pollut 205:385–393

    Article  CAS  Google Scholar 

  • Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: Implications for policy makers. Environ Sci Technol 45:1177–1183

    Article  CAS  Google Scholar 

  • Nyoka NWK, Kanyile SN, Bredenhand E, Prinsloo GJ, Otomo PV (2018) Biochar alleviates the toxicity of imidacloprid and silver nanoparticles (AgNPs) to Enchytraeus albidus (Oligochaeta). Environ Sci Pollut Res 25:10937–10945

    Article  CAS  Google Scholar 

  • O’Connor D, Peng T, Zhang J, Tsang DCW, Alessi DS, Shen Z, Bolan NS, Hou D (2018) Biochar application for the remediation of heavy metal polluted land: a review of in situ field trials. Sci Total Environ 619:815–826

    Article  CAS  Google Scholar 

  • OECD (2009) Guidelines for the Testing of Chemicals, No 232, Collembolan Reproduction Test in Soil. Organization for Economic Cooperation and Development, Paris

  • Paz-Ferreiro J, Nieto A, Méndez A, Askeland MPJ, Gascó G (2018) Biochar from Biosolids Pyrolysis: A Review. Int J Environ Res Public Health 15(5):956

    Article  CAS  Google Scholar 

  • Pohořelý M, Picek I, Skoblia S (2015) Apparatus for Multistage Gasification of Carbonaceous Fules. Pat. No. 306239/PV: 483. Applied: 15.07.09, Patented: 16.09.07

  • Prendergast-Miller MT, Duvall M, Sohi SP (2014) Biochar–root interactions are mediated by biochar nutrient content and impacts on soil nutrient availability. Eur J Soil Sci 65(1):173–185

    Article  CAS  Google Scholar 

  • Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: A review. Environ Toxicol Chem 18:89–108

    Article  CAS  Google Scholar 

  • Rodrigues NP, Scott-Fordsmand JJ, Amorim MJB (2020) Novel understanding of toxicity in a life cycle perspective–The mechanisms that lead to population effect–The case of Ag (nano) materials. Environ Pollut 262:114277

    Article  CAS  Google Scholar 

  • Roelofs D, Makama S, De Boer TE, Vooijs R, Van Gestel CAM, Van Den Brink NW (2020) Surface coating and particle size are main factors explaining the transcriptome-wide responses of the earthworm Lumbricus rubellus to silver nanoparticles. Environ Sci: Nano 7:1179–1193

    CAS  Google Scholar 

  • Salachna P, Byczyńska A, Zawadzińska A, Piechocki R, Mizielińska M (2019) Stimulatory effect of silver nanoparticles on the growth and flowering of potted oriental lilies. Agronomy 9:610

    Article  CAS  Google Scholar 

  • Saleeb N, Robinson B, Cavanagh J, Ross J, Munir K, Gooneratne R (2020) Antioxidant enzyme activity and lipid peroxidation in Aporrectodea caliginosa earthworms exposed to silver nanoparticles and silver nitrate in spiked soil. Environ Toxicol Chem 39:1257–1266

    Article  CAS  Google Scholar 

  • Shin YJ, Kwak JIl, An YJ, (2012) Evidence for the inhibitory effects of silver nanoparticles on the activities of soil exoenzymes. Chemosphere 88:524–529

    Article  CAS  Google Scholar 

  • Shirvanimoghaddam K, Czech B, Tyszczuk-Rotko K, Kończak M, Fakhrhoseini SM, Yadav R, Naebe M (2021) Sustainable synthesis of rose flower-like magnetic biochar from tea waste for environmental applications. J Adv Res In Press

  • Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011) Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida). Nanotoxicology 5:432–444

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research –WH Freeman and Co. New York, XIX

  • Stefaniuk M, Oleszczuk P, Bartmiński P (2016) Chemical and ecotoxicological evaluation of biochar produced from residues of biogas production. J Hazard Mater 318:417–424

    Article  CAS  Google Scholar 

  • Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76

    Article  CAS  Google Scholar 

  • Tang J, Zhu W, Kookana R, Katayama A (2013) Characteristics of biochar and its application in remediation of contaminated soil. J Biosci Bioeng 116:653–659

    Article  CAS  Google Scholar 

  • Tourinho PS, Loureiro S, Talluri VP, Dolar A, Verweij R, Chvojka J, Michalcová A, Kočí V, van Gestel CAM (2021) Microplastic fibers influence Ag toxicity and bioaccumulation in Eisenia andrei but not in Enchytraeus crypticus. Ecotoxicology 30:1216–1226

    Article  CAS  Google Scholar 

  • Velicogna JR, Ritchie EE, Scroggins RP, Princz JI (2016) A comparison of the effects of silver nanoparticles and silver nitrate on a suite of soil dwelling organisms in two field soils. Nanotoxicology 10:1144–1151

    Article  CAS  Google Scholar 

  • Waalewijn-Kool PL, Klein K, Forniés RM, van Gestel CAM (2014) Bioaccumulation and toxicity of silver nanoparticles and silver nitrate to the soil arthropod Folsomia candida. Ecotoxicology 23:1629–1637

    Article  CAS  Google Scholar 

  • Wan S, Li Y, Cheng S, Wu G, Yang X, Wang Y, Gao L (2022) Cadmium removal by FeOOH nanoparticles accommodated in biochar: Effect of the negatively charged functional groups in host. J Hazard Mater 421:126807

    Article  CAS  Google Scholar 

  • Weber K, Quicker P (2018) Properties of biochar. Fuel 217:240–261

    Article  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Yao Z, Li J, Xie H, Yu C (2012) Review on remediation technologies of soil contaminated by heavy metals. Procedia Environ Sci 16:722–729

    Article  CAS  Google Scholar 

  • Zhan F, Zeng W, Yuan X, Li B, Li T, Zu Y, Jiang M, Li Y (2019) Field experiment on the effects of sepiolite and biochar on the remediation of Cd-and Pb-polluted farmlands around a Pb–Zn mine in Yunnan Province, China. Environ Sci Pollut Res 26:7743–7751

    Article  CAS  Google Scholar 

  • Zhang X, Wang H, He L, Lu K, Sarmah A, Li J, Bolan NS, Pei J, Huang H (2013) Using biochar for remediation of soils contaminated with heavy metals and organic pollutants. Environ Sci Pollut Res 20:8472–8483

    Article  CAS  Google Scholar 

  • Zhao M, Dai Y, Zhang M, Feng C, Qin B, Zhang W, Zhao N, Li Y, Ni Z, Xu Z, Tsang DCW, Qiu R (2020) Mechanisms of Pb and/or Zn adsorption by different biochars: Biochar characteristics, stability, and binding energies. Sci Total Environ 717:136894

    Article  CAS  Google Scholar 

  • Zheng R, Chen Z, Cai C, Tie B, Liu X, Reid BJ, Huang Q, Lei M, Sun G, Baltrėnaitė E (2015) Mitigating heavy metal accumulation into rice (Oryza sativa L.) using biochar amendment—a field experiment in Hunan. China Environ Sci Pollut Res 22:11097–11108

    Article  CAS  Google Scholar 

  • Zhu X, Chen B, Zhu L, Xing B (2017) Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. Environ Pollut 227:98–115

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the European Structural and Investment Funds, OP RDE-funded project “CHEMFELLS4UCTP” (No. CZ.02.2.69/0.0/0.0/17_050/0008485), Ministry of Education, Youth and Sports of CR, European Regional Development Fund-Project “Centre for Experimental Plant Biology”: No. CZ.02.1.01/0.0/0.0/16_019/0000738, and specific university research—grant No. A1_FTOP_2021_004.

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K.A. Mocová was involved in conceptualization, data curation, formal analysis, investigation, methodology, visualization, writing—original draft. Š. Petrová helped in formal analysis, investigation, writing—review and editing. M. Pohořelý and M. Martinec contributed to methodology, writing—review and editing. P.S. Tourinho was involved in conceptualization, formal analysis, investigation, methodology, visualization, resources, writing—original draft. All authors edited, revised, and approved the final version of the manuscript.

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Correspondence to Klára Anna Mocová.

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Mocová, K.A., Petrová, Š., Pohořelý, M. et al. Biochar reduces the toxicity of silver to barley (Hordeum vulgare) and springtails (Folsomia candida) in a natural soil. Environ Sci Pollut Res 29, 37435–37444 (2022). https://doi.org/10.1007/s11356-021-18289-2

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