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Ecotoxicity of silver nanoparticles on plankton organisms: a review

  • Ioanna KalantziEmail author
  • Kyriaki Mylona
  • Claudio Toncelli
  • Thomas D. Bucheli
  • Katja Knauer
  • Spiros A. Pergantis
  • Paraskevi Pitta
  • Anastasia Tsiola
  • Manolis Tsapakis
Review
  • 122 Downloads

Abstract

Engineered silver nanoparticles (Ag-NPs) are ubiquitous in many commercial products due to their antibacterial and antifungal properties. Due to the different properties of NPs from their homolog bulk materials, the inevitable leaching of nanosilver from commercial products into the aquatic environment is raising concern about possible effects on aquatic organisms. This review aims at elucidating the inherent ecotoxicity of Ag-NPs for planktonic organisms that produce and transfer energy in the food web and play a key role in nutrient recycling. The current knowledge was gathered through laboratory studies on planktonic organisms, such as bacteria and algae. However, it has already been proven for other pollutants that the ecotoxicological response is strikingly different when simulating more realistic environmental conditions, as in the microcosm and mesocosm studies. Abiotic and biotic factors strongly contribute to altering the toxicity of Ag-NPs and of their released silver ions. The dilemma of the nano or ion effects of Ag-NP toxicity is hereby debated. As a general outlook, we observe that most of the studies were carried out at concentrations much higher than would ever be expected in the environment, and over time periods much shorter which would be typical for the environment. Furthermore, most of the research was focused on freshwater ecosystems and little information exists about the marine environment. It seems that Ag-NPs are less toxic than silver ions. Moreover, the Trojan Horse effect of Ag-NPs in the presence of other pollutants is poorly investigated. This review highlights these research gaps and recommends further research on the Ag-NP ecotoxicity in aquatic environments under more realistic conditions in large-scale experiments and their recovery from chemical stress.

Graphical abstract

Keywords

Ag-NPs Ecotoxicology Plankton Bacteria Mesocosms Microcosms Environmental effects 

Notes

Funding information

This research has been co-financed by the European Union and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework.

(NSRF)–ARISTEIA II (AQUANANO project, no. 4705).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11051_2019_4504_MOESM1_ESM.docx (214 kb)
ESM 1 (DOCX 214 kb)

References

  1. Allen HJ, Impellitteri CA, Macke DA et al (2010) Effects from filtration, capping agents, and presence/absence of food on the toxicity of silver nanoparticles to Daphnia magna. Environ Toxicol Chem 29:2742–2750.  https://doi.org/10.1002/etc.329 CrossRefGoogle Scholar
  2. Angel BM, Batley GE, Jarolimek CV, Rogers NJ (2013) The impact of size on the fate and toxicity of nanoparticulate silver in aquatic systems. Chemosphere 93:359–365.  https://doi.org/10.1016/j.chemosphere.2013.04.096 CrossRefGoogle Scholar
  3. Arnaout CL, Gunsch CK (2012) Impacts of silver nanoparticle coating on the nitrification potential of Nitrosomonas europaea. Environ Sci Technol 46:5387–5395CrossRefGoogle Scholar
  4. Aschberger K, Micheletti C, Sokull-Klüttgen B, Christensen FM (2011) Analysis of currently available data for characterising the risk of engineered nanomaterials to the environment and human health - lessons learned from four case studies. Environ Int 37:1143–1156.  https://doi.org/10.1016/j.envint.2011.02.005 CrossRefGoogle Scholar
  5. Asghari S, Johari SA, Lee JH et al (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanaobiotechnol 10:14.  https://doi.org/10.1186/1477-3155-10-14 CrossRefGoogle Scholar
  6. Auffan M, Rose J, Bottero J-Y et al (2009) Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634–641.  https://doi.org/10.1038/nnano.2009.242 CrossRefGoogle Scholar
  7. Baker TJ, Tyler CR, Galloway TS (2014) Impacts of metal and metal oxide nanoparticles on marine organisms. Environ Pollut 186:257–271.  https://doi.org/10.1016/j.envpol.2013.11.014 CrossRefGoogle Scholar
  8. Bao S, Wang H, Zhang W et al (2016) An investigation into the effects of silver nanoparticles on natural microbial communities in two freshwater sediments. Environ Pollut 219:696–704.  https://doi.org/10.1016/j.envpol.2016.06.071 CrossRefGoogle Scholar
  9. Baptista MS, Miller RJ, Halewood ER et al (2015) Impacts of silver nanoparticles on a natural estuarine plankton community. Environ Sci Technol 49:12968–12974.  https://doi.org/10.1021/acs.est.5b03285 CrossRefGoogle Scholar
  10. Batley GE, Kirby JK, Mclaughlin MJ (2013) Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res XXX: doi:  https://doi.org/10.1021/ar2003368 CrossRefGoogle Scholar
  11. Baun A, Hartmann NB, Grieger KD, Hansen SF (2009) Setting the limits for engineered nanoparticles in European surface waters - are current approaches appropriate? J Environ Monit 11:1774–1781.  https://doi.org/10.1039/b909730a CrossRefGoogle Scholar
  12. Becaro AA, Jonsson CM, Puti FC et al (2015) Toxicity of PVA-stabilized silver nanoparticles to algae and microcrustaceans. Environ Nanotechnol Monit Manage 3:22–29.  https://doi.org/10.1016/j.enmm.2014.11.002 CrossRefGoogle Scholar
  13. Beddow J, Stolpe B, Cole PA et al (2017) Nanosilver inhibits nitrification and reduces ammonia-oxidising bacterial but not archaeal amoA gene abundance in estuarine sediments. Environ Microbiol 19:500–510.  https://doi.org/10.1111/1462-2920.13441 CrossRefGoogle Scholar
  14. Bhatt I, Tripathi BN (2011) Interaction of engineered nanoparticles with various components of the environment and possible strategies for their risk assessment. Chemosphere 82:308–317.  https://doi.org/10.1016/j.chemosphere.2010.10.011 CrossRefGoogle Scholar
  15. Blakelock GC, Xenopoulos MA, Norman BC et al (2016) Effects of silver nanoparticles on bacterioplankton in a boreal lake. Freshw Biol 61:2211–2220.  https://doi.org/10.1111/fwb.12788 CrossRefGoogle Scholar
  16. Blaser SA, Scheringer M, MacLeod M, Hungerbühler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 390:396–409.  https://doi.org/10.1016/j.scitotenv.2007.10.010 CrossRefGoogle Scholar
  17. Boenigk J, Beisser D, Zimmermann S et al (2014) Effects of silver nitrate and silver nanoparticles on a planktonic community: general trends after short-term exposure. PLoS One 9:e95340.  https://doi.org/10.1371/journal.pone.0095340 CrossRefGoogle Scholar
  18. Bondarenko O, Juganson K, Ivask A et al (2013) Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–1200.  https://doi.org/10.1007/s00204-013-1079-4 CrossRefGoogle Scholar
  19. Bone AJ, Colman BP, Gondikas AP et al (2012) Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of Ag nanoparticles: part 2-toxicity and Ag speciation. Environ Sci Technol 46:6925–6933.  https://doi.org/10.1021/es204683m CrossRefGoogle Scholar
  20. Bone AJ, Matson CW, Colman BP et al (2015) Silver nanoparticle toxicity to Atlantic killifish (Fundulus heteroclitus) and Caenorhabditis elegans: a comparison of mesocosm, microcosm, and conventional laboratory studies. Environ Toxicol Chem 34:275–282.  https://doi.org/10.1002/etc.2806 CrossRefGoogle Scholar
  21. Borm PJA, Robbins D, Haubold S et al (2006) The potential risks of nanomaterials: a review carried out for ECETOC. Part Fibre Toxicol 3:11.  https://doi.org/10.1186/1743-8977-3-11 CrossRefGoogle Scholar
  22. Bour A, Mouchet F, Silvestre J et al (2015) Environmentally relevant approaches to assess nanoparticles ecotoxicity: a review. J Hazard Mater 283:764–777.  https://doi.org/10.1016/j.jhazmat.2014.10.021 CrossRefGoogle Scholar
  23. Boxall ABA, Chaudhry Q, Sinclair C, et al (2007) Current and future predicted environmental exposure to engineered nanoparticles. YorkGoogle Scholar
  24. Bradford A, Handy RD, Readman JW et al (2009) Impact of silver nanoparticle contamination on the genetic diversity of natural bacterial assemblages in estuarine sediments. Environ Sci Technol 43:4530–4536CrossRefGoogle Scholar
  25. Brock TCM, Crum SJH, Deneer JW et al (2004) Comparing aquatic risk assessment methods for the photosynthesis-inhibiting herbicides metribuzin and metamitron. Environ Pollut 130:403–426.  https://doi.org/10.1016/j.envpol.2003.12.022 CrossRefGoogle Scholar
  26. Bundschuh M, Filser J, Lüderwald S, et al (2018) Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur 30:. doi:  https://doi.org/10.1186/s12302-018-0132-6
  27. Burchardt AD, Carvalho RN, Valente A et al (2012) Effects of silver nanoparticles in diatom Thalassiosira pseudonana and Cyanobacterium Synechococcus sp. Environ Sci Technol.  https://doi.org/10.1021/es300989e CrossRefGoogle Scholar
  28. Button M, Auvinen H, Van Koetsem F et al (2016) Susceptibility of constructed wetland microbial communities to silver nanoparticles: a microcosm study. Ecol Eng 97:476–485.  https://doi.org/10.1016/j.ecoleng.2016.10.033 CrossRefGoogle Scholar
  29. Cairns J (1988) Putting the eco in ecotoxicology. Regul Toxicol Pharmacol 8:226–238CrossRefGoogle Scholar
  30. Caquet T, Lagadic L, Sheffield SR (2000) Reviews of environmental contamination and toxicology. Preface. Rev Environ Contam Toxicol 165:1–38Google Scholar
  31. Chae Y, An YJ (2016) Toxicity and transfer of polyvinylpyrrolidone-coated silver nanowires in an aquatic food chain consisting of algae, water fleas, and zebrafish. Aquat Toxicol 173:94–104.  https://doi.org/10.1016/j.aquatox.2016.01.011 CrossRefGoogle Scholar
  32. Chambers BA, Afrooz ARMN, Bae S et al (2014) Effects of chloride and ionic strength on physical morphology, dissolution, and bacterial toxicity of silver nanoparticles. Environ Sci Technol 48:761–769.  https://doi.org/10.1021/es403969x CrossRefGoogle Scholar
  33. Chapman PM, Fairbrother A, Brown D (1998) A critical evaluation of safety (uncertainty) factors for ecological risk assessment. Environ Toxicol Chem 17:99–108CrossRefGoogle Scholar
  34. Chen S, Jin Y, Lavoie M et al (2016) A new extracellular von Willebrand A domain-containing protein is involved in silver uptake in Microcystis aeruginosa exposed to silver nanoparticles. Appl Microbiol Biotechnol 100:8955–8963.  https://doi.org/10.1007/s00253-016-7728-9 CrossRefGoogle Scholar
  35. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588CrossRefGoogle Scholar
  36. Choi O, Deng KK, Kim N-J et al (2008) The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res 42:3066–3074.  https://doi.org/10.1016/j.watres.2008.02.021 CrossRefGoogle Scholar
  37. Choi O, Clevenger TE, Deng B et al (2009) Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res 43:1879–1886.  https://doi.org/10.1016/j.watres.2009.01.029 CrossRefGoogle Scholar
  38. Choi O, Yu C-P, Fernández EG et al (2010) Interactions of nanosilver with Escherichia coli cells in planktonic and biofilm cultures. Water Res 44:6095–6103.  https://doi.org/10.1016/j.watres.2010.06.069 CrossRefGoogle Scholar
  39. Cleveland D, Long SE, Pennington PL et al (2012) Pilot estuarine mesocosm study on the environmental fate of silver nanomaterials leached from consumer products. Sci Total Environ 421–422:267–272.  https://doi.org/10.1016/j.scitotenv.2012.01.025 CrossRefGoogle Scholar
  40. Coll C, Notter D, Gottschalk F et al (2016) Probabilistic environmental risk assessment of five nanomaterials (nano-TiO2, nano-Ag, nano-ZnO, CNT, and fullerenes). Nanotoxicology 10:436–444.  https://doi.org/10.3109/17435390.2015.1073812 CrossRefGoogle Scholar
  41. Colman BP, Espinasse B, Richardson CJ et al (2014) Emerging contaminant or an old toxin in disguise? Silver nanoparticle impacts on ecosystems. Environ Sci Technol 48:5229–5236.  https://doi.org/10.1021/es405454v CrossRefGoogle Scholar
  42. CPI (2018) CPI Home page - The Project on Emerging Nanotechnologies. Available athttp://www.nanotechproject.org/cpi/. Accessed on 05-09-2018
  43. Crane M, Handy RD, Garrod J, Owen R (2008) Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology 17:421–437.  https://doi.org/10.1007/s10646-008-0215-z CrossRefGoogle Scholar
  44. Cupi D, Hartmann NB, Baun A (2015) The influence of natural organic matter and aging on suspension stability in guideline toxicity testing of silver, zinc oxide, and titanium dioxide nanoparticles with Daphnia magna. Environ Toxicol Chem 34:497–506.  https://doi.org/10.1002/etc.2855 CrossRefGoogle Scholar
  45. Cupi D, Hartmann NB, Baun A (2016) Influence of pH and media composition on suspension stability of silver, zinc oxide, and titanium dioxide nanoparticles and immobilization of Daphnia magna under guideline testing conditions. Ecotoxicol Environ Saf 127:144–152.  https://doi.org/10.1016/j.ecoenv.2015.12.028 CrossRefGoogle Scholar
  46. Das P, Williams CJ, Fulthorpe RR et al (2012a) Changes in bacterial community structure after exposure to silver nanoparticles in natural waters. Environ Sci Technol 46:9120–9128.  https://doi.org/10.1021/es3019918 CrossRefGoogle Scholar
  47. Das P, Xenopoulos MA, Williams CJ et al (2012b) Effects of silver nanoparticles on bacterial activity in natural waters. Environ Toxicol Chem 31:122–130.  https://doi.org/10.1002/etc.716 CrossRefGoogle Scholar
  48. Das P, Xenopoulos MA, Metcalfe CD (2013) Toxicity of silver and titanium dioxide nanoparticle suspensions to the aquatic invertebrate, Daphnia magna. Bull Environ Contam Toxicol 91:76–82.  https://doi.org/10.1007/s00128-013-1015-6 CrossRefGoogle Scholar
  49. Das P, Metcalfe CD, Xenopoulos MA (2014) Interactive effects of silver nanoparticles and phosphorus on phytoplankton growth in natural waters. Environ Sci Technol 48:4573–4580.  https://doi.org/10.1021/es405039w CrossRefGoogle Scholar
  50. Dastjerdi R, Montazer M (2010) A review on the application of inorganic nano-structured materials in the modification of textiles: focus on anti-microbial properties. Colloids Surf B: Biointerfaces 79:5–18.  https://doi.org/10.1016/j.colsurfb.2010.03.029 CrossRefGoogle Scholar
  51. De La Torre-Roche R, Hawthorne J, Musante C et al (2012) Impact of Ag nanoparticle exposure on p,p’-DDE bioaccumulation by Cucurbita pepo (Zucchini) and Glycine max (Soybean). Environ Sci Technol 47:718–725.  https://doi.org/10.1021/es3041829 CrossRefGoogle Scholar
  52. Delay M, Frimmel FH (2012) Nanoparticles in aquatic systems. Anal Bioanal Chem 402:583–592.  https://doi.org/10.1007/s00216-011-5443-z CrossRefGoogle Scholar
  53. Dewez D, Oukarroum A (2012) Silver nanoparticles toxicity effect on photosystem II photochemistry of the green alga Chlamydomonas reinhardtii treated in light and dark conditions. Toxicol Environ Chem 94:1536–1546.  https://doi.org/10.1080/02772248.2012.712124 CrossRefGoogle Scholar
  54. Dobias J, Bernier-Latmani R (2013) Silver release from silver nanoparticles in natural waters. Environ Sci Technol 47:4140–4146.  https://doi.org/10.1021/es304023p CrossRefGoogle Scholar
  55. Doiron K, Pelletier E, Lemarchand K (2012) Impact of polymer-coated silver nanoparticles on marine microbial communities: a microcosm study. Aquat Toxicol 124–125:22–27.  https://doi.org/10.1016/j.aquatox.2012.07.004 CrossRefGoogle Scholar
  56. Echavarri-Bravo V, Paterson L, Aspray TJ et al (2017) Natural marine bacteria as model organisms for the hazard-assessment of consumer products containing silver nanoparticles. Mar Environ Res 130:293–302.  https://doi.org/10.1016/j.marenvres.2017.08.006 CrossRefGoogle Scholar
  57. Egorova EM (2011) Interaction of silver nanoparticles with biological objects: antimicrobial properties and toxicity for the other living organisms. J Phys Conf Ser 291:012050.  https://doi.org/10.1088/1742-6596/291/1/012050 CrossRefGoogle Scholar
  58. El Badawy AM, Silva RG, Morris B et al (2011) Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 45:283–287.  https://doi.org/10.1021/es1034188 CrossRefGoogle Scholar
  59. Escher BI, Hermens JLM (2004) Internal exposure: linking bioavailability to effects. Environ Sci Technol:455–462Google Scholar
  60. Exbrayat JM, Moudilou EN, Lapied E (2015) Harmful effects of nanoparticles on animals. J Nanotechnol 2015:1–10.  https://doi.org/10.1155/2015/861092 CrossRefGoogle Scholar
  61. Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009a) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290CrossRefGoogle Scholar
  62. Fabrega J, Renshaw JC, Lead JR (2009b) Interactions of silver nanoparticles with Pseudomonas putida biofilms. Environ Sci Technol 43:9004–9009.  https://doi.org/10.1021/es901706j CrossRefGoogle Scholar
  63. Fabrega J, Luoma SN, Tyler CR et al (2011a) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531.  https://doi.org/10.1016/j.envint.2010.10.012 CrossRefGoogle Scholar
  64. Fabrega J, Zhang R, Renshaw JC et al (2011b) Impact of silver nanoparticles on natural marine biofilm bacteria. Chemosphere 85:961–966.  https://doi.org/10.1016/j.chemosphere.2011.06.066 CrossRefGoogle Scholar
  65. Farkas J, Peter H, Christian P et al (2011) Characterization of the effluent from a nanosilver producing washing machine. Environ Int 37:1057–1062.  https://doi.org/10.1016/j.envint.2011.03.006 CrossRefGoogle Scholar
  66. Farré M, Gajda-Schrantz K, Kantiani L, Barceló D (2009) Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 393:81–95.  https://doi.org/10.1007/s00216-008-2458-1 CrossRefGoogle Scholar
  67. Feng QL, Wu J, Chen GQ et al (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52:662–668CrossRefGoogle Scholar
  68. Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233.  https://doi.org/10.1016/S0048-9697(03)00141-4 CrossRefGoogle Scholar
  69. Forbes VE, Calow P, Sibly RM (2001) Are current species extrapolation models a good basis for ecological risk assessment? Environ Toxicol Chem 20:442–447CrossRefGoogle Scholar
  70. Frens G, Overbeek JTG (1969) Carey Lea’s colloidal silver. Kolloid-Zeitschrift und Zeitschrift Fur Polym 922–929CrossRefGoogle Scholar
  71. Gambardella C, Costa E, Piazza V et al (2015) Effect of silver nanoparticles on marine organisms belonging to different trophic levels. Mar Environ Res 111:41–49.  https://doi.org/10.1016/j.marenvres.2015.06.001 CrossRefGoogle Scholar
  72. Gao J, Youn S, Hovsepyan A et al (2009) Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol 43:3322–3328CrossRefGoogle Scholar
  73. Garner KL, Keller AA (2014) Emerging patterns for engineered nanomaterials in the environment: a review of fate and toxicity studies. J Nanopart Res 16:1–28.  https://doi.org/10.1007/s11051-014-2503-2 CrossRefGoogle Scholar
  74. Garner KL, Suh S, Lenihan HS, Keller AA (2015) Species sensitivity distributions for engineered nanomaterials. Environ Sci Technol 49:5753–5759.  https://doi.org/10.1021/acs.est.5b00081 CrossRefGoogle Scholar
  75. Geranio L, Heuberger M, Nowack B (2009) The behavior of silver nanotextiles during washing. Environ Sci Technol 43:8113–8118.  https://doi.org/10.1021/es9018332 CrossRefGoogle Scholar
  76. Gil-Allué C, Schirmer K, Tlili A et al (2015) Silver nanoparticle effects on stream periphyton during short-term exposures. Environ Sci-Nano 49:1165–1172.  https://doi.org/10.1021/es5050166 CrossRefGoogle Scholar
  77. Gil-Allué C, Tlili A, Schirmer K et al (2018) Long-term exposure to silver nanoparticles affects periphyton community structure and function. Environ Sci-Nano 5:1397–1407.  https://doi.org/10.1039/C8EN00132D CrossRefGoogle Scholar
  78. Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222CrossRefGoogle Scholar
  79. Gottschalk F, Kost E, Nowack B (2013a) Engineered nanomaterials in water and soils: a risk quantification based on probabilistic exposure and effect modeling. Environ Toxicol Chem 32:1278–1287.  https://doi.org/10.1002/etc.2177 CrossRefGoogle Scholar
  80. Gottschalk F, Sun TY, Nowack B (2013b) Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environ Pollut 181:287–300.  https://doi.org/10.1016/j.envpol.2013.06.003 CrossRefGoogle Scholar
  81. Griffitt RJ, Luo J, Gao J et al (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978.  https://doi.org/10.1897/08-002.1 CrossRefGoogle Scholar
  82. Griffitt RJ, Hyndman K, Denslow ND, Barber DS (2009) Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 107:404–415.  https://doi.org/10.1093/toxsci/kfn256 CrossRefGoogle Scholar
  83. Grün AY, Meier J, Metreveli G et al (2016) Sublethal concentrations of silver nanoparticles affect the mechanical stability of biofilms. Environ Sci Pollut Res:24277–24288.  https://doi.org/10.1007/s11356-016-7691-0 CrossRefGoogle Scholar
  84. Gunsolus IL, Mousavi MPS, Hussein K et al (2015) Effects of humic and fulvic acids on silver nanoparticle stability, dissolution, and toxicity. Environ Sci Technol 49:8078–8086.  https://doi.org/10.1021/acs.est.5b01496 CrossRefGoogle Scholar
  85. Guo S, Wang E (2011) Noble metal nanomaterials: controllable synthesis and application in fuel cells and analytical sensors. Nano Today 6:240–264.  https://doi.org/10.1016/j.nantod.2011.04.007 CrossRefGoogle Scholar
  86. Guo Z, Chen G, Zeng G, et al (2016) Determination of inequable fate and toxicity of Ag nanoparticles in a Phanerochaete chrysosporium biofilm system through different sulfide sources. Environ Sci Nano doi:  https://doi.org/10.1039/C6EN00156D Google Scholar
  87. Harmon AR, Kennedy AJ, Poda AR et al (2014) Determination of nanosilver dissolution kinetics and toxicity in an environmentally relevant aqueous medium. Environ Toxicol Chem 33:1783–1791.  https://doi.org/10.1002/etc.2616 CrossRefGoogle Scholar
  88. Haulik B, Balla S, Palfi O et al (2015) Comparative ecotoxicity of the nano Ag, TiO2 and ZnO to aquatic species assemblages. Appl Ecol. Environ Res 13:325–338.  https://doi.org/10.15666/aeer/1302 CrossRefGoogle Scholar
  89. Hazani AA, Ibrahim MM, Shehata AI et al (2013) Ecotoxicity of Ag-nanoparticles on two microalgae, Chlorella vulgaris and Dunaliella tertiolecta. Arch Biol Sci 65:1447–1457.  https://doi.org/10.2298/ABS1304447H CrossRefGoogle Scholar
  90. He D, Dorantes-Aranda JJ, Waite TD (2012) Silver nanoparticle - algae interactions: oxidative dissolution, reactive oxygen species generation and synergistic toxic effects. Environ Sci Technol 46:8731–8738.  https://doi.org/10.1021/es300588a CrossRefGoogle Scholar
  91. Heinlaan M, Muna M, Knöbel M et al (2016) Natural water as the test medium for Ag and CuO nanoparticle hazard evaluation: an interlaboratory case study. Environ Pollut 216:689–699.  https://doi.org/10.1016/j.envpol.2016.06.033 CrossRefGoogle Scholar
  92. Hjorth R, Holden PA, Hansen SF et al (2017) The role of alternative testing strategies in environmental risk assessment of engineered nanomaterials. Environ Sci-Nano 4:292–301.  https://doi.org/10.1039/c6en00443a CrossRefGoogle Scholar
  93. Holden PA, Nisbet RM, Lenihan HS et al (2013) Ecological nanotoxicology: integrating nanomaterial hazard considerations across the subcellular, population, community, and ecosystems levels. Acc Chem Res 46:813–822.  https://doi.org/10.1021/ar300069t CrossRefGoogle Scholar
  94. Holden PA, Klaessig F, Turco RF et al (2014a) Evaluation of exposure concentrations used in assessing manufactured nanomaterial environmental hazards: are they relevant? Environ Sci Technol 48:10541–10551.  https://doi.org/10.1021/es502440s CrossRefGoogle Scholar
  95. Holden PA, Schimel JP, Godwin HA (2014b) Five reasons to use bacteria when assessing manufactured nanomaterial environmental hazards and fates. Curr Opin Biotechnol 27:73–78.  https://doi.org/10.1016/j.copbio.2013.11.008 CrossRefGoogle Scholar
  96. Holden PA, Gardea-Torresdey JL, Klaessig F et al (2016) Considerations of environmentally relevant test conditions for improved evaluation of ecological hazards of engineered nanomaterials. Environ Sci Technol 50:6124–6145.  https://doi.org/10.1021/acs.est.6b00608 CrossRefGoogle Scholar
  97. Hossain F, Perales-Perez OJ, Hwang S, Román F (2014) Antimicrobial nanomaterials as water disinfectant: applications, limitations and future perspectives. Sci Total Environ 466–467:1047–1059.  https://doi.org/10.1016/j.scitotenv.2013.08.009 CrossRefGoogle Scholar
  98. Hou W-C, Westerhoff P, Posner JD (2013) Biological accumulation of engineered nanomaterials: a review of current knowledge. Environ Sci Processes Impacts 15:103–122.  https://doi.org/10.1039/c2em30686g CrossRefGoogle Scholar
  99. Huang J, Cheng J, Yi J (2016a) Impact of silver nanoparticles on marine diatom Skeletonema costatum. J Appl Toxicol:1–12.  https://doi.org/10.1002/jat.3325 CrossRefGoogle Scholar
  100. Huang T, Sui M, Yan X et al (2016b) Anti-algae efficacy of silver nanoparticles to Microcystis aeruginosa: influence of NOM, divalent cations, and pH. Colloids Surf A Physicochem Eng Asp 509:492–503.  https://doi.org/10.1016/j.colsurfa.2016.09.009 CrossRefGoogle Scholar
  101. Hudson MLS (2013) Ecotoxicology of gold nanomaterials: effects on periphyton, L. stagnalis, and H. azteca in an aquatic food chain study. University of MichiganGoogle Scholar
  102. Ivask A, Juganson K, Bondarenko O et al (2014) Mechanisms of toxic action of Ag, ZnO and CuO nanoparticles to selected ecotoxicological test organisms and mammalian cells in vitro: a comparative review. Nanotoxicology 5390:1–15.  https://doi.org/10.3109/17435390.2013.855831 CrossRefGoogle Scholar
  103. Jain PK, Huang X, El-Sayed IH, El-Sayed MA (2008) Noble metals on the nanoscale: optical and photothermal properties and some applications in imaging, sensing, biology, and medicine. Acc Chem Res 41:1578–1586.  https://doi.org/10.1021/ar7002804 CrossRefGoogle Scholar
  104. Jemec A, Kahru A, Potthoff A et al (2016) An interlaboratory comparison of nanosilver characterisation and hazard identification: harmonising techniques for high quality data. Environ Int 87:20–32.  https://doi.org/10.1016/j.envint.2015.10.014 CrossRefGoogle Scholar
  105. Jiang HS, Yin L, Ren NN et al (2017) The effect of chronic silver nanoparticles on aquatic system in microcosms. Environ Pollut 223:395–402.  https://doi.org/10.1016/j.envpol.2017.01.036 CrossRefGoogle Scholar
  106. Kaegi R, Voegelin A, Sinnet B et al (2011) Behavior of metallic silver nanoparticles in a pilot wastewater treatment plant. Environ Sci Technol 45:3902–3908.  https://doi.org/10.1021/es1041892 CrossRefGoogle Scholar
  107. Kah M, Hofmann T (2014) Nanopesticide research: current trends and future priorities. Environ Int 63:224–235.  https://doi.org/10.1016/j.envint.2013.11.015 CrossRefGoogle Scholar
  108. Kahru A, Dubourguier H (2010) From ecotoxicology to nanoecotoxicology. Toxicology 269:105–119.  https://doi.org/10.1016/j.tox.2009.08.016 CrossRefGoogle Scholar
  109. Kaiser J-P, Zuin S, Wick P (2013) Is nanotechnology revolutionizing the paint and lacquer industry? A critical opinion. Sci Total Environ 442:282–289.  https://doi.org/10.1016/j.scitotenv.2012.10.009 CrossRefGoogle Scholar
  110. Kalwar K, Shan D (2018) Antimicrobial effect of silver nanoparticles (AgNPs) and their mechanism – a mini review. Micro Nano Lett 13:277–280.  https://doi.org/10.1049/mnl.2017.0648 CrossRefGoogle Scholar
  111. Kędziora A, Speruda M, Krzyżewska E et al (2018) Similarities and differences between silver ions and silver in nanoforms as antibacterial agents. Int J Mol Sci 19.  https://doi.org/10.3390/ijms19020444 CrossRefGoogle Scholar
  112. Kennedy AJ, Hull MS, Bednar AJ et al (2010) Fractionating nanosilver: importance for determining toxicity to aquatic test organisms. Environ Sci Technol 44:9571–9577.  https://doi.org/10.1021/es1025382 CrossRefGoogle Scholar
  113. Kim J, Van der Bruggen B (2010) The use of nanoparticles in polymeric and ceramic membrane structures: review of manufacturing procedures and performance improvement for water treatment. Environ Pollut 158:2335–2349.  https://doi.org/10.1016/j.envpol.2010.03.024 CrossRefGoogle Scholar
  114. Kim I, Lee BT, Kim HA et al (2016) Citrate coated silver nanoparticles change heavy metal toxicities and bioaccumulation of Daphnia magna. Chemosphere 143:99–105.  https://doi.org/10.1016/j.chemosphere.2015.06.046 CrossRefGoogle Scholar
  115. Klaine SJ, Alvarez PJJ, Batley GE et al (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851CrossRefGoogle Scholar
  116. Krzyzewska I, Kyzioł-Komosińska J, Rosik-Dulewska C et al (2016) Inorganic nanomaterials in the aquatic environment: behavior, toxicity, and interaction with environmental elements. Arch Environ Prot 42:87–101.  https://doi.org/10.1515/aep-2016-0011 CrossRefGoogle Scholar
  117. Książyk M, Asztemborska M, Stęborowski R, Bystrzejewska-Piotrowska G (2015) Toxic effect of silver and platinum nanoparticles toward the freshwater microalga Pseudokirchneriella subcapitata. Bull Environ Contam Toxicol 94:554–558.  https://doi.org/10.1007/s00128-015-1505-9 CrossRefGoogle Scholar
  118. Künniger T, Gerecke AC, Ulrich A et al (2014) Release and environmental impact of silver nanoparticles and conventional organic biocides from coated wooden façades. Environ Pollut 184:464–471.  https://doi.org/10.1016/j.envpol.2013.09.030 CrossRefGoogle Scholar
  119. Kvitek L, Vanickova M, Panacek A et al (2009) Initial study on the toxicity of silver nanoparticles (NPs) against Paramecium caudatum. J Phys Chem C 113:4296–4300CrossRefGoogle Scholar
  120. Lapresta-Fernández A, Fernández A, Blasco J (2012) Nanoecotoxicity effects of engineered silver and gold nanoparticles in aquatic organisms. TrAC Trends Anal Chem 32:40–59.  https://doi.org/10.1016/j.trac.2011.09.007 CrossRefGoogle Scholar
  121. Lea MC (1889) On allotroic forms of silver. Am J Sci 38:47–49CrossRefGoogle Scholar
  122. Lead JR, Batley GE, Alvarez PJJ et al (2018) Nanomaterials in the environment: behavior, fate, bioavailability, and effects—an updated review. Environ Toxicol Chem 37:2029–2063.  https://doi.org/10.1002/etc.4147 CrossRefGoogle Scholar
  123. Levard C, Hotze EM, Lowry GV, Brown GEJ (2012) Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol 46:6900–6914.  https://doi.org/10.1021/es2037405 CrossRefGoogle Scholar
  124. Levard C, Mitra S, Yang T et al (2013) Effect of chloride on the dissolution rate of silver nanoparticles and toxicity to E. coli. Environ Sci Technol 47:5738–5745.  https://doi.org/10.1021/es400396f CrossRefGoogle Scholar
  125. Li Y, Niu J, Shang E, Crittenden J (2014) Photochemical transformation and photoinduced toxicity reduction of silver nanoparticles in the presence of perfluorocarboxylic acids under UV irradiation. Environ Sci Technol 48:4946–4953.  https://doi.org/10.1021/es500596a CrossRefGoogle Scholar
  126. Li X, Schirmer K, Bernard L et al (2015) Silver nanoparticle toxicity and association with the alga Euglena gracilis. Environ Sci-Nano 2:594–602.  https://doi.org/10.1039/C5EN00093A CrossRefGoogle Scholar
  127. Liu Y, Tourbin M, Lachaize S, Guiraud P (2014) Nanoparticles in wastewaters: hazards, fate and remediation. Powder Technol 255:149–156.  https://doi.org/10.1016/j.powtec.2013.08.025 CrossRefGoogle Scholar
  128. Lohse SE, Murphy CJ (2012) Applications of colloidal inorganic nanoparticles: from medicine to energy. J Am Chem Soc 134:15607–15620.  https://doi.org/10.1021/ja307589n CrossRefGoogle Scholar
  129. Lok C, Ho C, Chen R et al (2006) Proteomic analysis of the mode of antibacterial action of silver research articles. J Proteome Res 5:916–924.  https://doi.org/10.1021/pr0504079 CrossRefGoogle Scholar
  130. Lok C-N, Ho C-M, Chen R et al (2007) Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–534.  https://doi.org/10.1007/s00775-007-0208-z CrossRefGoogle Scholar
  131. Lorenz C, Windler L, von Goetz N et al (2012) Characterization of silver release from commercially available functional (nano)textiles. Chemosphere 89:817–824.  https://doi.org/10.1016/j.chemosphere.2012.04.063 CrossRefGoogle Scholar
  132. Lowry GV, Gregory KB, Apte SC, Lead JR (2012) Transformations of nanomaterials in the environment. Environ Sci Technol 46:6893–6899.  https://doi.org/10.1021/es300839e CrossRefGoogle Scholar
  133. Luoma SN (2008) Silver nanotechnologies and the environment: old problems or new challenges? WoodrowWilsonInternational Center for Scholars, project on emerging nanotechnologies; The PEW Charitable Trusts, Washington, DC, USAGoogle Scholar
  134. Ma S, Lin D (2013) The biophysicochemical interactions at the interfaces between nanoparticles and aquatic organisms: adsorption and internalization. Environ Sci Processes Impacts 15:145–150.  https://doi.org/10.1039/c2em30637a CrossRefGoogle Scholar
  135. Mackevica A, Skjolding LM, Gergs A et al (2015) Chronic toxicity of silver nanoparticles to Daphnia magna under different feeding conditions. Aquat Toxicol 161:10–16.  https://doi.org/10.1016/j.aquatox.2015.01.023 CrossRefGoogle Scholar
  136. Marambio-Jones C, Hoek EMV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551.  https://doi.org/10.1007/s11051-010-9900-y CrossRefGoogle Scholar
  137. Markus AA, Parsons JR, Roex EWM et al (2016) Modelling the transport of engineered metallic nanoparticles in the river Rhine. Water Res 91:214–224.  https://doi.org/10.1016/j.watres.2016.01.003 CrossRefGoogle Scholar
  138. Massarsky A, Trudeau VL, Moon TW (2014) Predicting the environmental impact of nanosilver. Environ Toxicol Pharmacol 38:861–873.  https://doi.org/10.1016/j.etap.2014.10.006 CrossRefGoogle Scholar
  139. Matranga V, Corsi I (2012) Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar Environ Res 76:32–40.  https://doi.org/10.1016/j.marenvres.2012.01.006 CrossRefGoogle Scholar
  140. Matzke M, Jurkschat K, Backhaus T (2014) Toxicity of differently sized and coated silver nanoparticles to the bacterium Pseudomonas putida: risks for the aquatic environment? Ecotoxicology 23:818–829.  https://doi.org/10.1007/s10646-014-1222-x CrossRefGoogle Scholar
  141. McGillicuddy E, Murray I, Kavanagh S et al (2017) Silver nanoparticles in the environment: sources, detection and ecotoxicology. Sci Total Environ 575:231–246.  https://doi.org/10.1016/j.scitotenv.2016.10.041 CrossRefGoogle Scholar
  142. McLaughlin J, Bonzongo J-CJ (2012) Effects of natural water chemistry on nanosilver behavior and toxicity to Ceriodaphnia dubia and Pseudokirchneriella subcapitata. Environ Toxicol Chem 31:168–175.  https://doi.org/10.1002/etc.720 CrossRefGoogle Scholar
  143. McTeer J, Dean AP, White KN, Pittman JK (2014) Bioaccumulation of silver nanoparticles into Daphnia magna from a freshwater algal diet and the impact of phosphate availability. Nanotoxicology 8:305–316.  https://doi.org/10.3109/17435390.2013.778346 CrossRefGoogle Scholar
  144. Melo MAS, Guedes SFF, Xu HHK, Rodrigues LKA (2013) Nanotechnology-based restorative materials for dental caries management. Trends Biotechnol 31:459–467.  https://doi.org/10.1016/j.tibtech.2013.05.010 CrossRefGoogle Scholar
  145. Miao A-J, Schwehr KA, Xu C et al (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 157:3034–3041.  https://doi.org/10.1016/j.envpol.2009.05.047 CrossRefGoogle Scholar
  146. Miao A-J, Luo Z, Chen C-S et al (2010) Intracellular uptake: a possible mechanism for silver engineered nanoparticle toxicity to a freshwater alga Ochromonas danica. PLoS One 5:e15196.  https://doi.org/10.1371/journal.pone.0015196 CrossRefGoogle Scholar
  147. Miller RJ, Lenihan HS, Muller EB et al (2010) Impacts of metal oxide nanoparticles on marine phytoplankton. Environ Sci Technol 44:7329–7334.  https://doi.org/10.1021/es100247x CrossRefGoogle Scholar
  148. Minetto D, Volpi Ghirardini A, Libralato G (2016) Saltwater ecotoxicology of Ag, Au, CuO, TiO2, ZnO and C60 engineered nanoparticles: an overview. Environ Int 92–93:189–201.  https://doi.org/10.1016/j.envint.2016.03.041 CrossRefGoogle Scholar
  149. Mishra D, Hubenak JR, Mathur AB (2013) Nanoparticle systems as tools to improve drug delivery and therapeutic efficacy. J Biomed Mater Res A 101:3646–3660.  https://doi.org/10.1002/jbm.a.34642 CrossRefGoogle Scholar
  150. Mitrano DM, Ranville JF, Bednar A et al (2014) Tracking dissolution of silver nanoparticles at environmentally relevant concentrations in laboratory, natural, and processed waters using single particle ICP-MS (spICP-MS). Environ Sci-Nano 1:248.  https://doi.org/10.1039/c3en00108c CrossRefGoogle Scholar
  151. Moermond C, van Herwijnen R (2011) Environmental risk limits for silver in water. Natl Inst Public Heal Environ 1–45Google Scholar
  152. Money ES, Barton LE, Dawson J et al (2014) Validation and sensitivity of the FINE Bayesian network for forecasting aquatic exposure to nano-silver. Sci Total Environ 473–474:685–691.  https://doi.org/10.1016/j.scitotenv.2013.12.100 CrossRefGoogle Scholar
  153. Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–976.  https://doi.org/10.1016/j.envint.2006.06.014 CrossRefGoogle Scholar
  154. Moore JD, Stegemeier JP, Bibby K et al (2016) Impacts of pristine and transformed Ag and Cu engineered nanomaterials on surficial sediment microbial communities appear short-lived. Environ Sci Technol 50:2641–2651.  https://doi.org/10.1021/acs.est.5b05054 CrossRefGoogle Scholar
  155. Moreno-Garrido I, Perez S, Blasco J (2015) Toxicity of silver and gold nanoparticles on marine microalgae. Mar Environ Res 111:60–73.  https://doi.org/10.1016/j.marenvres.2015.05.008 CrossRefGoogle Scholar
  156. Morones JR, Elechiguerra JL, Camacho A et al (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353.  https://doi.org/10.1088/0957-4484/16/10/059 CrossRefGoogle Scholar
  157. Mortimer M, Gogos A, Bartolomé N et al (2014) Potential of hyperspectral imaging microscopy for semi-quantitative analysis of nanoparticle uptake by protozoa. Environ Sci Technol 48:8760–8767.  https://doi.org/10.1021/es500898j CrossRefGoogle Scholar
  158. Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453CrossRefGoogle Scholar
  159. Mueller-Spitz SR, Crawford KD (2014) Silver nanoparticle inhibition of polycyclic aromatic hydrocarbons degradation by Mycobacterium species RJGII-135. Lett Appl Microbiol 58:330–337.  https://doi.org/10.1111/lam.12205 CrossRefGoogle Scholar
  160. Navarro E, Baun A, Behra R et al (2008a) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386.  https://doi.org/10.1007/s10646-008-0214-0 CrossRefGoogle Scholar
  161. Navarro E, Piccapietra F, Wagner B et al (2008b) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964CrossRefGoogle Scholar
  162. Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627.  https://doi.org/10.1126/science.1114397 CrossRefGoogle Scholar
  163. Norman BC, Xenopoulos MA, Braun D, Frost PC (2015) Phosphorus availability alters the effects of silver nanoparticles on periphyton growth and stoichiometry. PLoS One 10:1–13.  https://doi.org/10.1371/journal.pone.0129328 CrossRefGoogle Scholar
  164. Notter DA, Mitrano DM, Nowack B (2014) Are nanosized or dissolved metals more toxic in the environment? A meta-analysis. Environ Toxicol Chem 33:2733–2739.  https://doi.org/10.1002/etc.2732 CrossRefGoogle Scholar
  165. Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22.  https://doi.org/10.1016/j.envpol.2007.06.006 CrossRefGoogle Scholar
  166. Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45:1177–1183.  https://doi.org/10.1021/es103316q CrossRefGoogle Scholar
  167. Oukarroum A, Bras S, Perreault F, Popovic R (2012a) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85.  https://doi.org/10.1016/j.ecoenv.2011.11.012 CrossRefGoogle Scholar
  168. Oukarroum A, Polchtchikov S, Perreault F, Popovic R (2012b) Temperature influence on silver nanoparticles inhibitory effect on photosystem II photochemistry in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Environ Sci Pollut Res Int 19:1755–1762.  https://doi.org/10.1007/s11356-011-0689-8 CrossRefGoogle Scholar
  169. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720.  https://doi.org/10.1128/AEM.02218-06 CrossRefGoogle Scholar
  170. Panacek A, Kvítek L, Prucek R et al (2006) Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 110:16248–16253.  https://doi.org/10.1021/jp063826h CrossRefGoogle Scholar
  171. Park S, Woodhall J, Ma G et al (2014) Regulatory ecotoxicity testing of engineered nanoparticles: are the results relevant to the natural environment? Nanotoxicology 8:583–592.  https://doi.org/10.3109/17435390.2013.818173 CrossRefGoogle Scholar
  172. Pascual García C, Burchardt AD, Carvalho RN et al (2014) Detection of silver nanoparticles inside marine diatom Thalassiosira pseudonana by electron microscopy and focused ion beam. PLoS One 9:e96078.  https://doi.org/10.1371/journal.pone.0096078 CrossRefGoogle Scholar
  173. Pasricha A, Jangra SL, Singh N et al (2012) Comparative study of leaching of silver nanoparticles from fabric and effective effluent treatment. J Environ Sci 24:852–859.  https://doi.org/10.1016/S1001-0742(11)60849-8 CrossRefGoogle Scholar
  174. Piccapietra F, Allué CG, Sigg L, Behra R (2012) Intracellular silver accumulation in Chlamydomonas reinhardtii upon exposure to carbonate coated silver nanoparticles and silver nitrate. Environ Sci Technol 46:7390–7397.  https://doi.org/10.1021/es300734m CrossRefGoogle Scholar
  175. Pletikapić G, Žutić V, Vinković Vrček I, Svetličić V (2012) Atomic force microscopy characterization of silver nanoparticles interactions with marine diatom cells and extracellular polymeric substance. J Mol Recognit 25:309–317.  https://doi.org/10.1002/jmr.2177 CrossRefGoogle Scholar
  176. Pokhrel LR, Dubey B, Scheuerman PR (2013) Impacts of select organic ligands on the colloidal stability, dissolution dynamics, and toxicity of silver nanoparticles. Environ Sci Technol 47:12877–12885.  https://doi.org/10.1021/es403462j CrossRefGoogle Scholar
  177. Pokhrel LR, Dubey B, Scheuerman PR (2014) Natural water chemistry (dissolved organic carbon, pH, and hardness) modulates colloidal stability, dissolution, and antimicrobial activity of citrate functionalized silver nanoparticles. Environ Sci-Nano 1:45–54CrossRefGoogle Scholar
  178. Preston BL (2002) Indirect effects in aquatic ecotoxicology: implications for ecological risk assessment. Environ Manag 29:311–323.  https://doi.org/10.1007/s00267-001-0023-1 CrossRefGoogle Scholar
  179. Qian H, Zhu K, Lu H et al (2016) Contrasting silver nanoparticle toxicity and detoxification strategies in Microcystis aeruginosa and Chlorella vulgaris: new insights from proteomic and physiological analyses. Sci Total Environ 572:1213–1221.  https://doi.org/10.1016/j.scitotenv.2016.08.039 CrossRefGoogle Scholar
  180. Quigg A, Chin W, Chen C et al (2013) Direct and indirect toxic effects of engineered nanoparticles on algae: role of natural organic matter. ACS Sustain Chem Eng 1:686–702.  https://doi.org/10.1021/sc400103x CrossRefGoogle Scholar
  181. Radzig MA, Nadtochenko VA, Koksharova OA et al (2013) Antibacterial effects of silver nanoparticles on gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloids Surf B: Biointerfaces 102:300–306.  https://doi.org/10.1016/j.colsurfb.2012.07.039 CrossRefGoogle Scholar
  182. Rai M, Ingle A (2012) Role of nanotechnology in agriculture with special reference to management of insect pests. Appl Microbiol Biotechnol 94:287–293.  https://doi.org/10.1007/s00253-012-3969-4 CrossRefGoogle Scholar
  183. Rai M, Kon K, Ingle A et al (2014) Broad-spectrum bioactivities of silver nanoparticles: the emerging trends and future prospects. Appl Microbiol Biotechnol 98:1951–1961.  https://doi.org/10.1007/s00253-013-5473-x CrossRefGoogle Scholar
  184. Reinsch BC, Levard C, Li Z et al (2012) Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ Sci Technol 46:6992–7000.  https://doi.org/10.1021/es203732x CrossRefGoogle Scholar
  185. Ribeiro F, Gallego-Urrea JA, Jurkschat K et al (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466–467:232–241.  https://doi.org/10.1016/j.scitotenv.2013.06.101 CrossRefGoogle Scholar
  186. Ribeiro F, Gallego-Urrea JA, Goodhead RM et al (2015) Uptake and elimination kinetics of silver nanoparticles and silver nitrate by Raphidocelis subcapitata: the influence of silver behaviour in solution. Nanotoxicology 9:1–10.  https://doi.org/10.3109/17435390.2014.963724 CrossRefGoogle Scholar
  187. Sakamoto M, Ha J-Y, Yoneshima S et al (2015) Free silver ion as the main cause of acute and chronic toxicity of silver nanoparticles to cladocerans. Arch Environ Contam Toxicol 68:500–509.  https://doi.org/10.1007/s00244-014-0091-x CrossRefGoogle Scholar
  188. Sakka Y, Skjolding LM, Mackevica A et al (2016) Behavior and chronic toxicity of two differently stabilized silver nanoparticles to Daphnia magna. Aquat Toxicol 177:526–535.  https://doi.org/10.1016/j.aquatox.2016.06.025 CrossRefGoogle Scholar
  189. Schaumann GE, Philippe A, Bundschuh M et al (2014) Understanding the fate and biological effects of Ag- and TiO2-nanoparticles in the environment: the quest for advanced analytics and interdisciplinary concepts. Sci Total Environ 535:3–19.  https://doi.org/10.1016/j.scitotenv.2014.10.035 CrossRefGoogle Scholar
  190. Schultz AG, Boyle D, Chamot D et al (2014) Aquatic toxicity of manufactured nanomaterials: challenges and recommendations for future toxicity testing. Environ Chem 11:207–226.  https://doi.org/10.1071/EN13221 CrossRefGoogle Scholar
  191. Scown TM, van Aerle R, Tyler CR (2010) Review: do engineered nanoparticles pose a significant threat to the aquatic environment? Crit Rev Toxicol 40:653–670.  https://doi.org/10.3109/10408444.2010.494174 CrossRefGoogle Scholar
  192. Sebastián M, Pitta P, González JM et al (2012) Bacterioplankton groups involved in the uptake of phosphate and dissolved organic phosphorus in a mesocosm experiment with P-starved Mediterranean waters. Environ Microbiol 14:2334–2347.  https://doi.org/10.1111/j.1462-2920.2012.02772.x CrossRefGoogle Scholar
  193. Selck H, Riemann B, Christoffersen K et al (2002) Comparing sensitivity of ecotoxicological effect endpoints between laboratory and field. Ecotoxicol Environ Saf 52:97–112.  https://doi.org/10.1006/eesa.2002.2172 CrossRefGoogle Scholar
  194. Sharma VK, Siskova KM, Zboril R, Gardea-Torresdey JL (2014) Organic-coated silver nanoparticles in biological and environmental conditions: fate, stability and toxicity. Adv Colloid Interf Sci 204:15–34.  https://doi.org/10.1016/j.cis.2013.12.002 CrossRefGoogle Scholar
  195. Sheng Z, Liu Y (2017) Potential impacts of silver nanoparticles on bacteria in the aquatic environment. J Environ Manag 191:290–296.  https://doi.org/10.1016/j.jenvman.2017.01.028 CrossRefGoogle Scholar
  196. Sigg L, Behra R, Groh K et al (2014) Chemical aspects of nanoparticle ecotoxicology. Chimia 68:806–811.  https://doi.org/10.2533/chimia.2014.806 CrossRefGoogle Scholar
  197. Silva T, Pokhrel LR, Dubey B et al (2014) Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: comparison between general linear model-predicted and observed toxicity. Sci Total Environ 468–469:968–976.  https://doi.org/10.1016/j.scitotenv.2013.09.006 CrossRefGoogle Scholar
  198. Sinouvassane D, Wong SL, Lim YM, Lee P (2016) A review on bio-distribution and toxicity of silver , titanium dioxide and zinc oxide nanoparticles in aquatic environment. Pollut Res 35:701–712Google Scholar
  199. Skoglund S, Lowe TA, Hedberg J et al (2013) Effect of laundry surfactants on surface charge and colloidal stability of silver nanoparticles. Langmuir 29:8882–8891.  https://doi.org/10.1021/la4012873 CrossRefGoogle Scholar
  200. Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275:177–182.  https://doi.org/10.1016/j.jcis.2004.02.012 CrossRefGoogle Scholar
  201. Sørensen SN, Lützhøft HCH, Rasmussen R, Baun A (2016) Acute and chronic effects from pulse exposure of D. magna to silver and copper nanoparticles. (submitted). Aquat Toxicol 180:209–217.  https://doi.org/10.1016/j.aquatox.2016.10.004 CrossRefGoogle Scholar
  202. Stevenson LM, Dickson H, Klanjscek T et al (2013) Environmental feedbacks and engineered nanoparticles: mitigation of silver nanoparticle toxicity to Chlamydomonas reinhardtii by algal-produced organic compounds. PLoS One 8:e74456.  https://doi.org/10.1371/journal.pone.0074456 CrossRefGoogle Scholar
  203. Stone L, Weisburd RSJ (1992) Positive feedback in aquatic ecosystems. Trends Ecol Evol 7:263–267.  https://doi.org/10.1016/0169-5347(92)90172-8 CrossRefGoogle Scholar
  204. Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76.  https://doi.org/10.1016/j.envpol.2013.10.004 CrossRefGoogle Scholar
  205. Suresh AK, Pelletier DA, Doktycz MJ (2013) Relating nanomaterials and microbial toxicity. Nanoscale 5:463–474CrossRefGoogle Scholar
  206. Swain P, Nayak SK, Sasmal A et al (2014) Antimicrobial activity of metal based nanoparticles against microbes associated with diseases in aquaculture. World J Microbiol Biotechnol 30:2491–2502.  https://doi.org/10.1007/s11274-014-1674-4 CrossRefGoogle Scholar
  207. Thiéry A, De Jong L, Issartel J et al (2012) Effects of metallic and metal oxide nanoparticles in aquatic and terrestrial food chains . Biomarkers responses in invertebrates and bacteria. Int J Nanotechnol 9:181–203CrossRefGoogle Scholar
  208. Thorley AJ, Tetley TD (2013) New perspectives in nanomedicine. Pharmacol Ther 140:176–185.  https://doi.org/10.1016/j.pharmthera.2013.06.008 CrossRefGoogle Scholar
  209. Tlili A, Jabiol J, Behra R et al (2017) Chronic exposure effects of silver nanoparticles on stream microbial decomposer communities and ecosystem functions. Environ Sci Technol 51:2447–2455.  https://doi.org/10.1021/acs.est.6b05508 CrossRefGoogle Scholar
  210. Toncelli C, Mylona K, Tsapakis M, Pergantis SA (2016) Flow injection with on-line dilution and single particle inductively coupled plasma – mass spectrometry for monitoring silver nanoparticles in seawater and in marine microorganisms. J Anal At Spectrom 31:1430–1439.  https://doi.org/10.1039/C6JA00011H CrossRefGoogle Scholar
  211. Tsiola A, Pitta P, Callol AJ et al (2017) The impact of silver nanoparticles on marine plankton dynamics: dependence on coating, size and concentration. Sci Total Environ 601–602:1838–1848.  https://doi.org/10.1016/j.scitotenv.2017.06.042 CrossRefGoogle Scholar
  212. Tsiola A, Toncelli C, Fodelianakis S et al (2018) Low-dose addition of silver nanoparticles stresses marine plankton communities. Environ Sci-Nano 4:2055–2065.  https://doi.org/10.1039/C8EN00195B CrossRefGoogle Scholar
  213. Tuominen M, Schultz E, Sillanpää M (2013) Toxicity and stability of silver nanoparticles to the green alga Pseudokirchneriella subcapitata in boreal freshwater samples and growth media. Nanomater Environ 1:48–57.  https://doi.org/10.2478/nanome-2013-0004 CrossRefGoogle Scholar
  214. Ulm L, Krivohlavek A, Jurasin D et al (2015) Response of biochemical biomarkers in the aquatic crustacean Daphnia magna exposed to silver nanoparticles. Environ Sci Pollut Res 22:19990–19999.  https://doi.org/10.1007/s11356-015-5201-4 CrossRefGoogle Scholar
  215. Van Aken B (2015) Gene expression changes in plants and microorganisms exposed to nanomaterials. Curr Opin Biotechnol 33:206–219.  https://doi.org/10.1016/j.copbio.2015.03.005 CrossRefGoogle Scholar
  216. Vance ME, Kuiken T, Vejerano EP et al (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780.  https://doi.org/10.3762/bjnano.6.181 CrossRefGoogle Scholar
  217. Vimbela GV, Ngo SM, Fraze C et al (2017) Antibacterial properties and toxicity from metallic nanomaterials. Int J Nanomedicine 12:3941–3965.  https://doi.org/10.2147/IJN.S134526 CrossRefGoogle Scholar
  218. Vincent JL, Paterson MJ, Norman BC et al (2017) Chronic and pulse exposure effects of silver nanoparticles on natural lake phytoplankton and zooplankton. Ecotoxicology 26:502–515.  https://doi.org/10.1007/s10646-017-1781-8 CrossRefGoogle Scholar
  219. Voelker D, Schlich K, Hohndorf L et al (2015) Approach on environmental risk assessment of nanosilver released from textiles. Environ Res 140:661–672.  https://doi.org/10.1016/j.envres.2015.05.011 CrossRefGoogle Scholar
  220. Völker C, Boedicker C, Daubenthaler J et al (2013a) Comparative toxicity assessment of nanosilver on three Daphnia species in acute, chronic and multi-generation experiments. PLoS One 8:e75026.  https://doi.org/10.1371/journal.pone.0075026 CrossRefGoogle Scholar
  221. Völker C, Oetken M, Oehlmann J (2013b) The biological effects and possible modes of action of nanosilver. Rev Environ Contam Toxicol 223:81–106.  https://doi.org/10.1007/978-1-4614-5577-6 CrossRefGoogle Scholar
  222. von Moos N, Slaveykova VI (2014) Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae - state of the art and knowledge gaps. Environ Sci-Nano 8:605–630.  https://doi.org/10.3109/17435390.2013.809810 CrossRefGoogle Scholar
  223. von Moos N, Bowen P, Slaveykova VI (2014) Bioavailability of inorganic nanoparticles to planktonic bacteria and aquatic microalgae in freshwater. Environ Sci-Nano 1:214–232.  https://doi.org/10.1039/c3en00054k CrossRefGoogle Scholar
  224. Walters CR, Pool EJ, Somerset VS (2014) Ecotoxicity of silver nanomaterials in the aquatic environment: a review of literature and gaps in nano-toxicological research. J Environ Sci Health A 49:1588–1601.  https://doi.org/10.1080/10934529.2014.938536 CrossRefGoogle Scholar
  225. Wang Z, Chen J, Li X et al (2012) Aquatic toxicity of nanosilver colloids to different trophic organisms: contributions of particles and free silver ion. Environ Toxicol Chem 31:2408–2413.  https://doi.org/10.1002/etc.1964 CrossRefGoogle Scholar
  226. Wang Z, Quik JTK, Song L et al (2015) Humic substances alleviate the aquatic toxicity of polyvinylpyrrolidone-coated silver nanoparticles to organisms of different trophic levels. Environ Toxicol Chem 34:1239–1245.  https://doi.org/10.1002/etc.2936 CrossRefGoogle Scholar
  227. Wiesner MR, Lowry GV, Alvarez P et al (2006) Assessing the risks of manufactured nanomaterials. Environ Sci Technol 40:4336–4345CrossRefGoogle Scholar
  228. Wirth SM, Lowry GV, Tilton RD (2012) Natural organic matter alters biofilm tolerance to silver nanoparticles and dissolved silver. Environ Sci Technol 46:12687–12696.  https://doi.org/10.1021/es301521p CrossRefGoogle Scholar
  229. Wirth SM, Bertuccio AJ, Cao F et al (2016) Inhibition of bacterial surface colonization by immobilized silver nanoparticles depends critically on the planktonic bacterial concentration. J Colloid Interface Sci 467:17–27.  https://doi.org/10.1016/j.jcis.2015.12.049 CrossRefGoogle Scholar
  230. Wise K, Brasuel M (2011) The current state of engineered nanomaterials in consumer goods and waste streams: the need to develop nanoproperty-quantifiable sensors for monitoring engineered nanomaterials. Nanotechnol Sci Appl 4:73–86.  https://doi.org/10.2147/NSA.S9039 CrossRefGoogle Scholar
  231. Wu F, Harper BJ, Harper SL (2017) Differential dissolution and toxicity of surface functionalized silver nanoparticles in small-scale microcosms: impacts of community complexity. Environ Sci-Nano 4:359–372.  https://doi.org/10.1039/c6en00324a CrossRefGoogle Scholar
  232. Yu S, Chao J, Sun J et al (2013a) Quantification of the uptake of silver nanoparticles and ions to HepG2 cells. Environ Sci Technol 47:3268–3274.  https://doi.org/10.1021/es304346p CrossRefGoogle Scholar
  233. Yu S, Yin Y, Liu J (2013b) Silver nanoparticles in the environment. Environ Sci Processes Impacts 15:78–92.  https://doi.org/10.1039/c2em30595j CrossRefGoogle Scholar
  234. Zhang Z, Yang X, Shen M et al (2015) Sunlight-driven reduction of silver ion to silver nanoparticle by organic matter mitigates the acute toxicity of silver to Daphnia magna. J Environ Sci (China) 35:62–68.  https://doi.org/10.1016/j.jes.2015.03.007 CrossRefGoogle Scholar
  235. Zhang C, Hu Z, Deng B (2016a) Silver nanoparticles in aquatic environments: physiochemical behavior and antimicrobial mechanisms. Water Res 88:403–427.  https://doi.org/10.1016/j.watres.2015.10.025 CrossRefGoogle Scholar
  236. Zhang L, Li J, Yang K et al (2016b) Physicochemical transformation and algal toxicity of engineered nanoparticles in surface water samples. Environ Pollut 211:132–140.  https://doi.org/10.1016/j.envpol.2015.12.041 CrossRefGoogle Scholar
  237. Zhang W, Xiao B, Fang T (2018) Chemical transformation of silver nanoparticles in aquatic environments: mechanism, morphology and toxicity. Chemosphere 191:324–334.  https://doi.org/10.1016/j.chemosphere.2017.10.016 CrossRefGoogle Scholar
  238. Zhao C-M, Wang W-X (2010) Biokinetic uptake and efflux of silver nanoparticles in Daphnia magna. Environ Sci Technol 44:7699–7704.  https://doi.org/10.1021/es101484s CrossRefGoogle Scholar
  239. Zhao C-M, Wang W-X (2011) Comparison of acute and chronic toxicity of silver nanoparticles and silver nitrate to Daphnia magna. Environ Toxicol Chem 30:885–892.  https://doi.org/10.1002/etc.451 CrossRefGoogle Scholar
  240. Zou X, Shi J, Zhang H (2014) Coexistence of silver and titanium dioxide nanoparticles: enhancing or reducing environmental risks? Aquat Toxicol 154:168–175.  https://doi.org/10.1016/j.aquatox.2014.05.020 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Ioanna Kalantzi
    • 1
    Email author
  • Kyriaki Mylona
    • 1
  • Claudio Toncelli
    • 1
    • 2
    • 3
  • Thomas D. Bucheli
    • 4
  • Katja Knauer
    • 5
  • Spiros A. Pergantis
    • 2
  • Paraskevi Pitta
    • 1
  • Anastasia Tsiola
    • 1
  • Manolis Tsapakis
    • 1
  1. 1.Institute of OceanographyHellenic Centre for Marine ResearchHeraklionGreece
  2. 2.Environmental Chemical Processes Laboratory, Department of ChemistryUniversity of CreteHeraklionGreece
  3. 3.Laboratory of Biomimetic Membranes and Textiles, Empa, Swiss Federal Laboratories for Materials Science and TechnologySt. GallenSwitzerland
  4. 4.Environmental Analytics, AgroscopeZürichSwitzerland
  5. 5.Federal Office of AgricultureBernSwitzerland

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