Polyvinylpyrrolidone and arsenic-induced changes in biological responses of model aquatic organisms exposed to iron-based nanoparticles

  • Verónica Llaneza
  • Ismael Rodea-Palomares
  • Zuo Zhou
  • Roberto Rosal
  • Francisca Fernández-Pina
  • Jean-Claude J. BonzongoEmail author
Research Paper


The efficiency of zero-valent iron particles used in the remediation of contaminated groundwater has, with the emergence of nanotechnology, stimulated interest on the use of nano-size particles to take advantage of high-specific surface area and reactivity characteristics of nanoparticles (NPs). Accordingly, engineered iron-NPs are among the most widely used nanomaterials for in situ remediation. However, while several ecotoxicity studies have been conducted to investigate the adverse impacts of these NPs on aquatic organisms, research on the implications of spent iron-based NPs is lacking. In this study, a comparative approach is used, in which the biological effects of three iron-based NPs (Fe3O4 and γ-Fe2O3 NPs with particle sizes ranging from 20 to 50 nm, and Fe0-NPs with an average particle size of 40 nm) on Raphidocelis subcapitata (formely known as Pseudokirchneriella subcapitata) and Daphnia magna were investigated using both as-prepared and pollutant-doped Fe-based NPs. For the latter, arsenic (As) was used as example sorbed pollutant. The results show that improved degree of NP dispersion by use of polyvinylpyrrolidone overlapped with both increased arsenic adsorption capacity and toxicity to the tested organisms. For R. subcapitata, Fe-oxide NPs were more toxic than Fe0-NPs, due primarily to differences in the degree of NPs aggregation and ability to produce reactive oxygen species. For the invertebrate D. magna, a similar trend of biological responses was observed, except that sorption of As to Fe0-NPs significantly increased the toxic response when compared to R. subcapitata. Overall, these findings point to the need for research on downstream implications of NP-pollutant complexes generated during water treatment by injection of NPs into aquatic systems.


Iron Nanoparticles Arsenic Algae Invertebrate Toxicity Environmental effects 



This research was supported by a seed grant from the University of Florida to JCB. VL was supported by the Bridge to the Doctorate Fellowship from the Office of Graduate Minority Programs in addition to a UF-Alumni Assistantship. We thank Joseph Marchionno from UF and Jennifer Quiros Jimenez of the Universidad de Alcalá for their help with different lab experiments and sample analysis. Finally, the authors thank the anonymous reviewers who helped improve the overall quality of the manuscript.

Supplementary material

11051_2016_3541_MOESM1_ESM.docx (5 mb)
Supplementary material 1 (DOCX 5070 kb)


  1. Adeleye AS, Keller AA, Miller RJ, Lenihan HS (2013) Persistence of commercial nano-scaled zero-valent iron (nZVI) and by-products. J Nanopart Res 15(1):1–18CrossRefGoogle Scholar
  2. Adeleye AS, Stevenson LM, Su Y, Nisbet RM, Zhang Y, Keller AA (2016) Influence of phytoplankton on fate and effects of modified zero-valent iron nanoparticles. Environ Sci Technol. doi: 10.1021/acs.est.5b06251 Google Scholar
  3. Auffan MI, Achouak W, Rose JRM, Roncato M-A, Chaneac C, Waite DT, Masion A, Woicik JC, Wiesner MR, Bottero J-Y (2008) Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli. Environ Sci Technol 42(17):6730–6735CrossRefGoogle Scholar
  4. Cao J, Zhang W-X (2006) Stabilization of chromium ore processing residue (COPR) with nanoscale iron particles. J Hazard Mater 132(2–3):213–219CrossRefGoogle Scholar
  5. Chen J, Xiu Z, Lowry GV, Alvarez PJJ (2011) Effect of natural organic matter on toxicity and reactivity of nano-scale zero-valent iron. Water Res 45(5):1995–2001CrossRefGoogle Scholar
  6. Chen Z, Yin J-J, Zhou Y-T, Zhang Y, Song L, Song M, Hu S, Gu N (2012) Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano 6(5):4001–4012CrossRefGoogle Scholar
  7. Chertok B, David AE, Yang VC (2010) Polyethyleneimine-modified iron oxide nanoparticles for brain tumor drug delivery using magnetic targeting and intra-carotid administration. Biomaterials 31(24):6317–6324CrossRefGoogle Scholar
  8. Cornell S (1996) The iron oxides; structure, properties, reactions, occurrence and uses, 1st edn. VCH, New YorkGoogle Scholar
  9. Crane RA, Dickinson M, Popescu IC, Scott TB (2011) Magnetite and zero-valent iron nanoparticles for the remediation of uranium contaminated environmental water. Water Res 45:2931–2942CrossRefGoogle Scholar
  10. Dabrunz A, Duester L, Prasse C, Seitz F, Rosenfeldt R, Schilde C, Schaumann GE, Schulz R (2011) Biological surface coating and molting inhibition as mechanisms of tio2 nanoparticle toxicity in Daphnia magna. PLOS One 6(5):e20112CrossRefGoogle Scholar
  11. Dixit S, Hering JG (2003) Comparison of As(V) and As(III) sorption onto iron oxide minerals: implications for arsenic mobility. Environ Sci Technol 37(18):4182–4189CrossRefGoogle Scholar
  12. Fang Z, Chen J, Qiu X, Qiu X, Cheng W, Zhu L (2011) Effective removal of antibiotic metronidazole from water by nanoscale zero-valent iron particles. Desalination 268(1–3):60–67CrossRefGoogle Scholar
  13. Gao J, Wang Y, Hovsepyan A, Bonzongo J-C (2011) Effects of engineered nanomaterials on microbial catalyzed biogeochemical processes in sediments. J Hazard Mater 186(1):940–945CrossRefGoogle Scholar
  14. Gong N, Shao K, Feng W, Lin Z, Liang C, Sun Y (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83(4):510–516CrossRefGoogle Scholar
  15. Gonzalo S, Llaneza V, Pulido-Reyes G, Fernández-Piñas F, Bonzongo J-C, Leganes F, Rosal R, Garcia-Calvo E, Rodea-Palomares I (2014) A colloidal singularity reveals the crucial role of colloidal stability for nanomaterials in vitro toxicity testing: nZVI-microalgae colloidal system as a case study. PLOS One 9(10):e109645CrossRefGoogle Scholar
  16. Gorski CA, Nurmi JT, Tratnyek PG, Hofstetter TB, Scherer MM (2009) Redox behavior of magnetite: implications for contaminant reduction. Environ Sci Technol 44(1):55–60CrossRefGoogle Scholar
  17. Gregory J (2006) Particles in water properties and processes. Taylor & Francis, Boca Raton, p 180Google Scholar
  18. Grieger KD, Fjordbøge A, Hartmann NB, Eriksson E, Bjerg PL, Baun A (2010) Environmental benefits and risks of zero-valent iron nanoparticles (nZVI) for in situ remediation: risk mitigation or trade-off? J Contam Hydrol 118(3–4):165–183CrossRefGoogle Scholar
  19. Gupta A, Curtis AG (2004) Surface modified superparamagnetic nanoparticles for drug delivery: interaction studies with human fibroblasts in culture. J Mater Sci Mater Med 15(4):493–496CrossRefGoogle Scholar
  20. He F, Zhao D (2007) Manipulating the size and dispersibility of zerovalent iron nanoparticles by use of carboxymethyl cellulose stabilizers. Environ Sci Technol 41(17):6216–6221CrossRefGoogle Scholar
  21. Huang Q, Shi X, Pinto RA, Petersen EJ, Weber WJ (2008) Tunable synthesis and immobilization of zero-valent iron nanoparticles for environmental applications. Environ Sci Technol 42(23):8884–8889CrossRefGoogle Scholar
  22. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133(1):1–16CrossRefGoogle Scholar
  23. Hwang Y, Kim D, Ahn Y-T, Moon C-M, Shin H-S (2012) Recovery of ammonium salt from nitrate-containing water by Iron nanoparticles and membrane contactor. Environ Eng Res 17:111–116CrossRefGoogle Scholar
  24. Johnson RL, Johnson GOB, Nurmi JT, Tratnyek PG (2009) Natural organic matter enhanced mobility of nano zerovalent iron. Environ Sci Technol 43(14):5455–5460CrossRefGoogle Scholar
  25. Kim H, Hong H-J, Jung J, Kim S-H, Yang J-W (2010a) Degradation of trichloroethylene (TCE) by nanoscale zero-valent iron (nZVI) immobilized in alginate bead. J Hazard Mater 176(1–3):1038–1043CrossRefGoogle Scholar
  26. Kim JY, Park HJ, Lee C, Nelson KL, Sedlak DL, Yoon J (2010b) Inactivation of Escherichia coli by nanoparticulate zerovalent iron and ferrous ion. Appl Environ Microbiol 76:7668–7670CrossRefGoogle Scholar
  27. Lavicoli I, Fontana L, Leso V, Calabrese EJ (2014) Hormetic dose-responses in nanotechnology studies. Sci Total Environ 487:361–374CrossRefGoogle Scholar
  28. Lee C, Kim JY, Lee WI, Nelson KL, Yoon J, Sedlak DL (2008) Bactericidal effect of zero-valent iron nanoparticles on Escherichia coli. Environ Sci Technol 42(13):4927–4933CrossRefGoogle Scholar
  29. Li X-Q, Zhang WX (2006) Iron nanoparticles: the core-shell structure and unique properties for Ni(II) sequestration. Langmuir 22(10):4638–4642CrossRefGoogle Scholar
  30. Ma S, Lin D (2013) The biophysicochemical interactions at the interfaces between nanoparticles and aquatic organisms: adsorption and internalization. Environ Sci Process Impact 15(1):145–160CrossRefGoogle Scholar
  31. Macé C, Desrocher S, Gheorghiu F, Kane A, Pupeza M, Cernik M, Kvapil P, Venkatakrishnan R, Zhang W-X (2006) Nanotechnology and groundwater remediation: a step forward in technology understanding. Remediat J 16(2):23–33CrossRefGoogle Scholar
  32. Malynych S, Luzinov I, Chumanov G (2002) Poly(Vinyl Pyridine) as a universal surface modifier for immobilization of nanoparticles. J Phys Chem B 106(6):1280–1285CrossRefGoogle Scholar
  33. Moreau JW, Weber PK, Martin MC, Gilbert B, Hutcheon ID, Banfield JF (2007) Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 316(5831):1600–1603CrossRefGoogle Scholar
  34. Mostafa MG, Chen Y-H, Jean J-S, Liu C-C, Lee Y-C (2011) Kinetics and mechanism of arsenate removal by nanosized iron oxide-coated perlite. J Hazard Mater 187:89–95CrossRefGoogle Scholar
  35. Mueller NC, Braun J, Bruns J, Černík M, Rissing P, Rickerby D, Nowack B (2012) Application of nanoscale zero valent iron (nZVI) for groundwater remediation in Europe. Environ Sci Pollut Res 19(2):550–558CrossRefGoogle Scholar
  36. Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nano-level. Science 311(5761):622–627CrossRefGoogle Scholar
  37. Oberdorster G, Oberdorster E, Oberdorster J (2007) Concepts of nanoparticle dose metric and response metric. Environ Health Perspect 115(6):A290CrossRefGoogle Scholar
  38. OECD (2004) Test no. 202: Daphnia sp. acute immobilisation test. OECD Publishing, ParisCrossRefGoogle Scholar
  39. Olegario JT, Yee N, Miller M, Sczepaniak J, Manning B (2009) Reduction of Se(VI) to Se(-II) by zerovalent iron nanoparticle suspensions. J Nanopart Res 12(6):2057–2068CrossRefGoogle Scholar
  40. Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13(2):45–49CrossRefGoogle Scholar
  41. Phenrat T, Saleh N, Sirk K, Tilton RD, Lowry GV (2006) Aggregation and sedimentation of aqueous nanoscale zerovalent iron dispersions. Environ Sci Technol 41(1):284–290CrossRefGoogle Scholar
  42. Pisanic tr, Blackwell JD, Shubayev VI, Finones RR, Jin S (2007) Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 28(16):2572–2581CrossRefGoogle Scholar
  43. Ponder SM, Darab JG, Mallouk TE (2000) Remediation of Cr(VI) and Pb(II) aqueous solutions using supported, nanoscale zero-valent iron. Environ Sci Technol 34(12):2564–2569CrossRefGoogle Scholar
  44. Rodea-Palomares I, Gonzalo S, Santiago-Morales J, Leganés F, García-Calvo E, Rosal R, Fernández-Piñas F (2012) An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms. Aquat Toxicol 122–123:133–143CrossRefGoogle Scholar
  45. Sadiq IM, Dalai S, Chandrasekaran N, Mukherjee A (2011a) Ecotoxicity study of titania (TiO2) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotoxicol Environ Saf 74(5):1180–1187CrossRefGoogle Scholar
  46. Sadiq IM, Pakrashi S, Chandrasekaran N, Mukherjee A (2011b) Studies on toxicity of aluminum oxide (Al2O3) nanoparticles to microalgae species: Scenedesmus sp. and Chlorella sp. J Nanopart Res 13(8):3287–3299CrossRefGoogle Scholar
  47. Sakulchaicharoen N, O’Carroll DM, Herrera JE (2010) Enhanced stability and de-chlorination activity of pre-synthesis stabilized nanoscale FePd particles. J Contam Hydrol 118(3–4):117–127CrossRefGoogle Scholar
  48. Saleh N, Kim H-J, Phenrat T, Matyjaszewski K, Tilton RD, Lowry GV (2008) Ionic strength and composition affect the mobility of surface-modified fe0 nanoparticles in water-saturated sand columns. Environ Sci Technol 42(9):3349–3355CrossRefGoogle Scholar
  49. Scott TB, Dickinson M, Crane RA, Riba O, Hughes GM, Allen GC (2010) The effects of vacuum annealing on the structure and surface chemistry of iron nanoparticles. J Nanopart Res 12:1765–1775CrossRefGoogle Scholar
  50. Sharma VK, Sohn M (2009) Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ Int 35(4):743–759CrossRefGoogle Scholar
  51. Shin K-H, Cha DK (2008) Microbial reduction of nitrate in the presence of nanoscale zero-valent iron. Chemosphere 72(2):257–262CrossRefGoogle Scholar
  52. Sidhu PS (1981) Dissolution of iron oxides and oxyhydroxides in hydrochloric and perchloric acids. Clay Clay Miner 29(4):269–276CrossRefGoogle Scholar
  53. Sun Y-P, Li X-Q, Cao J, Zhang W-X, Wang HP (2006) Characterization of zero-valent iron nanoparticles. Adv Colloid Interface Sci 120(1–3):47–56CrossRefGoogle Scholar
  54. US-EPA (2002) Test method 1003.0—Green algae, Selenastrum capriconutum, GrowthGoogle Scholar
  55. Vernon JD, Bonzongo J-CJ (2014) Volatilization and sorption of dissolved mercury by metallic iron of different particle sizes: implications for treatment of mercury contaminated water effluents. J Hazard Mater 276:408–414CrossRefGoogle Scholar
  56. Voinov MA, Pagan JOS, Morrison E, Smirnova TI, Smirnov AI (2010) Surface-mediated production of hydroxyl radicals as a mechanism of iron oxide nanoparticle biotoxicity. J Am Chem Soc 133(1):35–41CrossRefGoogle Scholar
  57. Warheit DB, Hoke RA, Finlay C, Donner EM, Reed KL, Sayes CM (2007) Development of a base set of toxicity tests using ultrafine TiO2 particles as a component of nanoparticle risk management. Toxicol Lett 171(3):99–110CrossRefGoogle Scholar
  58. Wu H, Yin J-J, Wamer WG, Zeng M, Lo YM (2014) Reactive oxygen species-related activities of nano-iron metal and nano-iron oxides. J Food Drug Anal 22(1):86–94CrossRefGoogle Scholar
  59. Xiu Z-M, Gregory KB, Lowry GV, Alvarez PJJ (2010) Effect of bare and coated nanoscale zerovalent iron on tceA and vcrA gene expression in Dehalococcoides spp. Environ Sci Technol 44(19):7647–7651CrossRefGoogle Scholar
  60. Yang X, Hong H, Grailer JJ, Rowland IJ, Javadi A, Hurley SA, Xiao Y, Yang Y, Zhang Y, Nickles RJ, Cai W, Steeber DA, Gong S (2011) cRGD-functionalized, DOX-conjugated, and 64Cu-labeled superparamagnetic iron oxide nanoparticles for targeted anticancer drug delivery and PET/MR imaging. Biomaterials 32(17):4151–4160CrossRefGoogle Scholar
  61. Zhang W-X (2003) Nanoscale iron particles for environmental remediation: an overview. J Nanopart Res 5(3):323–332CrossRefGoogle Scholar
  62. Zhang Y, Sun C, Kohler N, Zhang M (2004) Self-assembled coatings on individual monodisperse magnetite nanoparticles for efficient intracellular uptake. Biomed Microdevice 6(1):33–40CrossRefGoogle Scholar
  63. Zhao X, Liu W, Cai Z, Han B, Qian T, Zhao D (2016) An overview of preparation and applications of stabilized zero-valent iron nanoparticles for soil and groundwater remediation. Water res 100:245–266CrossRefGoogle Scholar
  64. Zhaunerchyk V, Geppert WD, Rosen S, Vigren E, Hamberg M, Kamińska M, Kashperka I, af Ugglas M, Semaniak J, Larsson M, Thomas RD (2009) Investigation into the vibrational yield of OH products in the OH+ H+ H channel arising from the dissociative recombination of H3O+. J Chem Phys 130:214302CrossRefGoogle Scholar
  65. Zhu X, Chang Y, Chen Y (2010) Toxicity and bioaccumulation of TiO2 nanoparticle aggregates in Daphnia magna. Chemosphere 78(3):209–215CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Engineering School of Sustainable Infrastructure and Environment, Department of Environmental Engineering SciencesUniversity of FloridaGainesvilleUSA
  2. 2.Dept. de Biologia, Facultad de CienciasUniv. Autonoma de MadridMadridSpain
  3. 3.Dept. de Ingeniería QuímicaUniv. de AlcaláAlcalá de HenaresSpain

Personalised recommendations