Skip to main content
Log in

Translocation and biotoxicity of metal (oxide) nanoparticles in the wetland-plant system

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Engineered nanoparticles (ENPs) threaten the environment through wastewater discharging. Generally, constructed wetlands (CWs) are efficient methods for ENPs removal. However, the biotoxicity of ENPs on plants in CWs is unclear. Here, we investigated the distribution and bio-impacts of different ENPs (Ag NPs, TiO2 NPs, and CeO2 NPs) in plants under 5- and 60-day exposure to 1 and 50 mg/L concentrations. Results showed that ENPs appeared in the vascular bundle and mesophyll cell space, which induced the variation in antioxidase activities (e.g., superoxide dismutase [SOD], peroxidase [POD], and catalase [CAT] activities) as well as overproduction of malondialdehyde (MDA). Additionally, Ag NPs inhibited photosynthesis rate and root activity during two exposure phases. CeO2 NPs had positive and negative impacts on plants in 5- and 60-day exposure, respectively. Inversely, TiO2 NPs enhanced photosynthesis and root activity under 60-day exposure. Finally, the contents of the C, N, and P elements in plants fluctuated in response to ENPs stress. All results have a positive correlation with the wetland performance under ENPs exposure except for TiO2 NPs treatment. Overall, our study systematically reveals aquatic plants’ responses to ENPs and provides a reference for building ecological treatment systems to purify wastewater containing ENPs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ali M, Cheng Z, Ahmad H, Hayat S (2018). Reactive oxygen species (ROS) as defenses against a broad range of plant fungal infections and case study on ROS employed by crops against Verticillium dahliae wilts. Journal of Plant Interactions, 13(1): 353–363

    Article  CAS  Google Scholar 

  • Auvinen H, Sepulveda V V, Rousseau D P L, Du Laing G (2016). Substrate- and plant-mediated removal of citrate-coated silver nanoparticles in constructed wetlands. Environmental Science and Pollution Research International, 23(21): 21920–21926

    Article  CAS  Google Scholar 

  • Backhausen J E, Kitzmann C, Horton P, Scheibe R (2000). Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons. Photosynthesis Research, 64(1): 1–13

    Article  CAS  Google Scholar 

  • Barrios A C, Rico C M, Trujillo-Reyes J, Medina-Velo I A, Peralta-Videa J R, Gardea-Torresdey J L (2016). Effects of uncoated and citric acid coated cerium oxide nanoparticles, bulk cerium oxide, cerium acetate, and citric acid on tomato plants. Science of the Total Environment, 563: 956–964

    Article  Google Scholar 

  • Bour A, Mouchet F, Cadarsi S, Silvestre J, Chauvet E, Bonzom J M, Pagnout C, Clivot H, Gauthier L, Pinelli E (2016). Impact of CeO2 nanoparticles on the functions of freshwater ecosystems: A microcosm study. Environmental Science. Nano, 3(4): 830–838

    Article  CAS  Google Scholar 

  • Coll C, Notter D, Gottschalk F, Sun T, Som C, Nowack B (2016). Probabilistic environmental risk assessment of five nanomaterials (nano-TiO2, nano-Ag, nano-ZnO, CNT, and fullerenes). Nanotoxicology, 10(4): 436–444

    Article  CAS  Google Scholar 

  • Conway J R, Beaulieu A L, Beaulieu N L, Mazer S J, Keller A A (2015). Environmental stresses increase photosynthetic disruption by metal oxide nanomaterials in a soil-grown plant. ACS Nano, 9(12): 11737–11749

    Article  CAS  Google Scholar 

  • Corral-Diaz B, Peralta-Videa J R, Alvarez-Parrilla E, Rodrigo-García J, Morales M I, Osuna-Avila P, Niu G, Hernandez-Viezcas J A, Gardea-Torresdey J L (2014). Cerium oxide nanoparticles alter the antioxidant capacity but do not impact tuber ionome in Raphanus sativus (L). Plant Physiology and Biochemistry, 84: 277–285

    Article  CAS  Google Scholar 

  • Dietz K J, Herth S (2011). Plant nanotoxicology. Trends in Plant Science, 16(11): 582–589

    Article  CAS  Google Scholar 

  • Dronova I, Gong P, Clinton N E, Wang L, Fu W, Qi S, Liu Y (2012). Landscape analysis of wetland plant functional types: The effects of image segmentation scale, vegetation classes and classification methods. Remote Sensing of Environment, 127: 357–369

    Article  Google Scholar 

  • Du W, Gardea-Torresdey J L, Ji R, Yin Y, Zhu J, Peralta-Videa J R, Guo H (2015). Physiological and biochemical changes imposed by CeO2 nanoparticles on wheat: A life cycle field study. Environmental Science & Technology, 49(19): 11884–11893

    Article  CAS  Google Scholar 

  • Foltête A S, Masfaraud J F, Bigorgne E, Nahmani J, Chaurand P, Botta C, Labille J, Rose J, Ferard J F, Cotelle S (2011). Environmental impact of sunscreen nanomaterials: Ecotoxicity and genotoxicity of altered TiO2 nanocomposites on Vicia faba. Environmental Pollution, 159(10): 2515–2522

    Article  Google Scholar 

  • Gao J, Xu G, Qian H, Liu P, Zhao P, Hu Y (2013). Effects of nano-TiO2 on photosynthetic characteristics of Ulmus elongata seedlings. Environmental Pollution, 176: 63–70

    Article  CAS  Google Scholar 

  • García-Gómez C, García S, Obrador A, Almendros P, González D, Fernández M D. (2020). Effect of ageing of bare and coated nanoparticles of zinc oxide applied to soil on the Zn behaviour and toxicity to fish cells due to transfer from soil to water bodies. Science of the Total Environment, 706: 135713

    Article  Google Scholar 

  • Gottschalk F, Sonderer T, Scholz R W, Nowack B (2009). Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, Fullerenes) for different regions. Environmental Science & Technology, 43(24): 9216–9222

    Article  CAS  Google Scholar 

  • He Y, Yu C, Zhou L, Chen Y, Liu A, Jin J, Hong J, Qi Y, Jiang D (2014). Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max.) under salt stress. Plant Physiology and Biochemistry, 74: 118–124

    Article  CAS  Google Scholar 

  • Hendren C O, Badireddy A R, Casman E, Wiesner M R (2013). Modeling nanomaterial fate in wastewater treatment: Monte Carlo simulation of silver nanoparticles (nano-Ag). Science of the Total Environment, 449: 418–425

    Article  CAS  Google Scholar 

  • Hong F H, Zhou J, Liu C, Yang F, Wu C, Zheng L, Yang P (2005). Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biological Trace Element Research, 105(1–3): 269–279

    Article  CAS  Google Scholar 

  • Hu X, Liu X, Yang X, Guo F, Su X, Chen Y (2018). Acute and chronic responses of macrophyte and microorganisms in constructed wetlands to cerium dioxide nanoparticles: Implications for wastewater treatment. Chemical Engineering Journal, 348: 35–45

    Article  CAS  Google Scholar 

  • Huang J, Cao C, Yan C, Liu J, Hu Q, Guan W (2017). Impacts of silver nanoparticles on the nutrient removal and functional bacterial community in vertical subsurface flow constructed wetlands. Bioresource Technology, 243: 1216–1226

    Article  CAS  Google Scholar 

  • Huang J, Cheng J, Yi J (2016). Impact of silver nanoparticles on marine diatom Skeletonema costatum. Journal of Applied Toxicology, 36 (10): 1343–1354

    Article  CAS  Google Scholar 

  • Jacob D L, Borchardt J D, Navaratnam L, Otte M L, Bezbaruah A N (2013). Uptake and translocation of ti from nanoparticles in crops and wetland plants. International Journal of Phytoremediation, 15(2): 142–153

    Article  CAS  Google Scholar 

  • Katerova Z, Todorova D (2011). Effect of enhanced UV-C irradiation on the growth, malondialdehyde, hydrogen peroxide, free proline, polyamines, iaa and iaa-oxidase activity in pea plants (pisum sativum l.). Comptes Rendus De L Academie Bulgare Des Sciences, 64(11): 1555–1562

    CAS  Google Scholar 

  • Ke M J, Qu Q, Peijnenburg W, Li X X, Zhang M, Zhang Z Y, Lu T, Pan X L, Qian H F (2018). Phytotoxic effects of silver nanoparticles and silver ions to Arabidopsis thaliana as revealed by analysis of molecular responses and of metabolic pathways. Science of the Total Environment, 644: 1070–1079

    Article  CAS  Google Scholar 

  • Kong L, Wang Y B, Zhao L N, Chen Z H (2009). Enzyme and root activities in surface-flow constructed wetlands. Chemosphere, 76(5): 601–608

    Article  CAS  Google Scholar 

  • Lee W M, An Y J (2013). Effects of zinc oxide and titanium dioxide nanoparticles on green algae under visible, UVA, and UVB irradiations: No evidence of enhanced algal toxicity under UV pre-irradiation. Chemosphere, 91(4): 536–544

    Article  CAS  Google Scholar 

  • Lyu S, Wei X, Chen J, Wang C, Wang X, Pan D (2017). Titanium as a beneficial element for crop production. Frontiers of Plant Science, 8: 597

    Article  Google Scholar 

  • Ma H B, Brennan A, Diamond S A (2012). Photocatalytic reactive oxygen species production and phototoxicity of titanium dioxide nanoparticles are dependent on the solar ultraviolet radiation spectrum. Environmental Toxicology and Chemistry, 31(9): 2099–2107

    Article  CAS  Google Scholar 

  • Majumdar S, Peralta-Videa J R, Trujillo-Reyes J, Sun Y, Barrios A C, Niu G, Margez J P F, Gardea-Torresdey J L. (2016). Soil organic matter influences cerium translocation and physiological processes in kidney bean plants exposed to cerium oxide nanoparticles. Science of the Total Environment, 569: 201–211

    Article  Google Scholar 

  • Matorin D N, Todorenko D A, Seifullina N K, Zayadan B K, Rubin A B (2013). Effect of silver nanoparticles on the parameters of chlorophyll fluorescence and P-700 reaction in the green alga Chlamydomonas reinhardtii. Microbiology, 82(6): 809–814

    Article  CAS  Google Scholar 

  • Movafeghi A, Khataee A, Abedi M, Tarrahi R, Dadpour M, Vafaei F (2018). Effects of TiO2 nanoparticles on the aquatic plant Spirodela polyrrhiza: Evaluation of growth parameters, pigment contents and antioxidant enzyme activities. Journal of Environmental Sciences (China), 64: 130–138

    Article  CAS  Google Scholar 

  • Qi J, Song C P, Wang B, Zhou J, Kangasjarvi J, Zhu J K, Gong Z (2018). Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. Journal of Integrative Plant Biology, 60(9): 805–826

    Article  CAS  Google Scholar 

  • Queiroz A M, Mezacasa A V, Graciano D E, Falco W F, M’peko J C, Guimaraes F E G, Lawson T, Colbeck I, Oliveira S L, Caires A R L (2016). Quenching of chlorophyll fluorescence induced by silver nanoparticles. Spectrochimica Acta Part a-Molecular and Biomolecular Spectroscopy, 168: 73–77

    Article  CAS  Google Scholar 

  • Rico C M, Morales M I, Mccreary R, Castillo-Michel H, Barrios A C, Hong J, Tafoya A, Lee W Y, Varela-Ramirez A, Peralta-Videa J R, Gardea-Torresdey J L (2013). Cerium oxide nanoparticles modify the antioxidative stress enzyme activities and macromolecule composition in rice seedlings. Environmental Science & Technology, 47(24): 14110–14118

    Article  CAS  Google Scholar 

  • Roy B, Chandrasekaran H, Palamadai Krishnan S, Chandrasekaran N, Mukherjee A. (2018). UVI pre-irradiation to P25 titanium dioxide nanoparticles enhanced its toxicity towards freshwater algae Scenedesmus obliquus. Environmental Science and Pollution Research International, 25(17): 16729–16742

    Article  CAS  Google Scholar 

  • Sarmast M K, Salehi H (2016). Silver nanoparticles: An influential element in plant nanobiotechnology. Molecular Biotechnology, 58 (7): 441–449

    Article  CAS  Google Scholar 

  • Schwabe F, Schulin R, Limbach L K, Stark W, Bürge D, Nowack B. (2013). Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture. Chemosphere, 91(4): 512–520

    Article  CAS  Google Scholar 

  • Stottmeister U, Wiessner A, Kuschk P, Kappelmeyer U, Kastner M, Bederski O, Muller R A, Moormann H (2003). Effects of plants and microorganisms in constructed wetlands for wastewater treatment. Biotechnology Advances, 22(1–2): 93–117

    Article  CAS  Google Scholar 

  • Su M, Hong F, Liu C, Wu X, Liu X, Chen L, Gao F, Yang F, Li Z (2007). Effects of nano-anatase TiO2 on absorption, distribution of light, and photoreduction activities of chloroplast membrane of spinach. Biological Trace Element Research, 118(2): 120–130

    Article  CAS  Google Scholar 

  • Thwala M, Musee N, Sikhwivhilu L, Wepener V (2013). The oxidative toxicity of Ag and ZnO nanoparticles towards the aquatic plant Spirodela punctuta and the role of testing media parameters. Environmental Science. Processes & Impacts, 15(10): 1830–1843

    Article  CAS  Google Scholar 

  • Torabian S, Zahedi M, Khoshgoftar A H (2016). Effects of foliar spray of two kinds of zinc oxide on the growth and ion concentration of sunflower cultivars under salt stress. Journal of Plant Nutrition, 39(2): 172–180

    Article  CAS  Google Scholar 

  • Trujillo-Reyes J, Majumdar S, Botez C E, Peralta-Videa J R, Gardea-Torresdey J L (2014). Exposure studies of core-shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: Are they a potential physiological and nutritional hazard? Journal of Hazardous Materials, 267: 255–263

    Article  CAS  Google Scholar 

  • Vymazal J (2007). Removal of nutrients in various types of constructed wetlands. Science of the Total Environment, 380(1–3): 48–65

    Article  CAS  Google Scholar 

  • Wang C, Zhang H, Ruan L, Chen L, Li H, Chang X L, Zhang X, Yang S T (2016a). Bioaccumulation of 13C-fullerenol nanomaterials in wheat. Environmental Science. Nano, 3(4): 799–805

    Article  CAS  Google Scholar 

  • Wang X, Liu Y, Zhang H, Shen X, Cai F, Zhang M, Gao Q, Chen W, Wang B, Tao S (2016b). The impact of carbon nanotubes on bioaccumulation and translocation of phenanthrene, 3-CH3-phenanthrene and 9-NO2-phenanthrene in maize (Zea mays) seedlings. Environmental Science. Nano, 3(4): 818–829

    Article  CAS  Google Scholar 

  • Wang X P, Yang X Y, Chen S Y, Li Q Q, Wang W, Hou C J, Gao X, Wang L, Wang S C (2016c). Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis. Frontiers of Plant Science, 6: 1243

    Article  Google Scholar 

  • Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008). Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiology and Biochemistry, 46(8–9): 786–793

    Article  CAS  Google Scholar 

  • Yang F, Hong F S, You W J, Liu C, Gao F Q, Wu C, Yang P (2006). Influences of nano-anatase TiO2 on the nitrogen metabolism of growing spinach. Biological Trace Element Research, 110(2): 179–190

    Article  CAS  Google Scholar 

  • Yang X, Chen Y, Liu X, Guo F, Su X, He Q (2018). Influence of titanium dioxide nanoparticles on functionalities of constructed wetlands for wastewater treatment. Chemical Engineering Journal, 352: 655–663

    Article  CAS  Google Scholar 

  • Yang X, He Q, Guo F, Sun X, Zhang J, Chen M, Vymazal J, Chen Y (2020a). Nanoplastics disturb nitrogen removal in constructed wetlands: Responses of microbes and macrophytes. Environmental Science & Technology, 54(21): 14007–14016

    Article  CAS  Google Scholar 

  • Yang X, He Q, Guo F, Sun X, Zhang J, Chen Y (2021). Impacts of carbon-based nanomaterials on nutrient removal in constructed wetlands: Microbial community structure, enzyme activities, and metabolism process. Journal of Hazardous Materials, 401: 123270

    Article  CAS  Google Scholar 

  • Yang X Y, Chen Y, Guo F C, Liu X B, Su X X, He Q (2020b). Metagenomic analysis of the biotoxicity of titanium dioxide nanoparticles to microbial nitrogen transformation in constructed wetlands. Journal of Hazardous Materials, 384: 121376

    Article  CAS  Google Scholar 

  • Ye Y, Medina-Velo I A, Cota-Ruiz K, Moreno-Olivas F, Gardea-Torresdey J L (2019). Can abiotic stresses in plants be alleviated by manganese nanoparticles or compounds? Ecotoxicology and Environmental Safety, 184: 109671

    Article  CAS  Google Scholar 

  • Zhang H, Huang M, Zhang W, Gardea-Torresdey J L, White J C, Ji R, Zhao L (2020). Silver nanoparticles alter soil microbial community compositions and metabolite profiles in implanted and cucumber-planted soils. Environmental Science & Technology, 54(6): 3334–3342

    Article  CAS  Google Scholar 

  • Zhang H, He X, Zhang Z, Zhang P, Li Y, Ma Y, Kuang Y, Zhao Y, Chai Z (2011a). Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environmental Science & Technology, 45 (8): 3725–3730

    Article  CAS  Google Scholar 

  • Zhang M, Smith J, Harberd N, Jiang C. (2016a). The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Molecular Biology, 91(6): 651–659

    Article  CAS  Google Scholar 

  • Zhang P, Ma Y, Zhang Z, He X, Zhang J, Guo Z, Tai R, Zhao Y, Chai Z (2012). Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano, 6(11): 9943–9950

    Article  CAS  Google Scholar 

  • Zhang Y Q, Dringen R, Petters C, Rastedt W, Koser J, Filser J, Stolte S (2016b). Toxicity of dimercaptosuccinate-coated and un-functionalized magnetic iron oxide nanoparticles towards aquatic organisms. Environmental Science. Nano, 3(4): 754–767

    Article  CAS  Google Scholar 

  • Zhang Z, He X, Zhang H, Ma Y, Zhang P, Ding Y, Zhao Y (2011b). Uptake and distribution of ceria nanoparticles in cucumber plants. Metallomics, 3(8): 816–822

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 51708056), the National Major Project of Pollution Control and Treatment Science and Technology (Grant No. 2017ZX07401003-4), and Chongqing Talents Plan for Young Talents (No. CQY201905062). We also thank the Analytical and Testing Center of Chongqing University for SEM and TEM imaging.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yi Chen.

Additional information

Highlights

• Aquatic plants are more likely to absorb TiO2 NPs that are beneficial to them.

• Ag NPs inhibited the growth of aquatic plants under both 5- and 60-day exposure.

• CeO2 NPs had positive/negative impact on plant in 5/60-day exposure, respectively.

• TiO2 NPs presence could enhance the photosynthesis and increase the plant biomass.

• The ENPs changed plant activity, which resulted in changes of wetland performance.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, X., He, Q., Guo, F. et al. Translocation and biotoxicity of metal (oxide) nanoparticles in the wetland-plant system. Front. Environ. Sci. Eng. 15, 138 (2021). https://doi.org/10.1007/s11783-021-1432-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-021-1432-4

Keywords

Navigation