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

Abstract

• 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.

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.

Graphical abstract

Keywords

Constructed wetlands / Aquatic plants / Nanoparticles / Physiological activity / Biomass

References

[1] 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

[2] 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

[3] 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

[4] 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

[5] 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

[6] 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

[7] 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

[8] 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

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

[10] 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

[11] 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

[12] 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

[13] 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

[14] 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

[15] 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

[16] 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

[17] 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

[18] 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

[19] 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

[20] 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

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

[22] 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

[23] 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

[24] 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

[25] 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

[26] 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

[27] 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

[28] 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

[29] 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

[30] 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

[31] 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

[32] 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

[33] 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

[34] 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

[35] 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

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

[37] 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

[38] 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

[39] 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

[40] 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

[41] 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

[42] 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

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

[44] 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

[45] 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

[46] 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

[47] 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

[48] 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

[49] 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

[50] 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

[51] 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

[52] 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

[53] 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

[54] 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 unplanted and cucumber-planted soils. Environmental Science & Technology, 54(6): ‏ 3334–3342

[55] 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

[56] 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

[57] 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

[58] 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

[59] 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

RIGHTS & PERMISSIONS

Higher Education Press