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Toxicological Effects Induced by Silver Nanoparticles in Zebra Fish (Danio Rerio) and in the Bacteria Communities Living at Their Surface

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Abstract

The antimicrobial activity of silver nanoparticles (AgNP) makes them useful in a wide range of products although their environmental impact is still uncertain. The main goal of this study was to evaluate short-term effects induced by AgNP on gills oxidative status and bacterial communities living at the skin mucus of zebrafish. Both the number of bacteria colony forming units and bacteria growth obtained from skin mucus were lower in all concentrations tested (25, 50 and 100 µg nAg/L). Besides, AgNP exposure caused a significant decrease in bacteria growth in zebrafish exposed to 100 µg nAg/L. AgNP accumulated in zebrafish gills at both highest concentrations tested, but this accumulation did not appear to result in oxidative stress. Overall the results indicated toxicological effects of AgNP on bacteria communities living at the zebrafish mucus surface. Although silver accumulation was verified in gills, no evidence of toxicity in terms of oxidative stress was found.

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References

  • Ahamed M, AlSalhi MS, Siddiqui MKJ (2010) Silver nanoparticle applications and human health. Clin Chim Acta 411:1841–1848. doi:10.1016/j.cca.2010.08.016

    Article  CAS  Google Scholar 

  • Amado LL, Longaray Garcia M, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123. doi:10.1016/j.scitotenv.2008.11.038

    Article  CAS  Google Scholar 

  • AshaRani PV, Prakash Hande M, Valiyaveettil S (2009) Anti-proliferative activity of silver nanoparticles. BMC Cell Biol 10:65. doi:10.1186/1471-2121-10-65 http://www.biomedcentral.com/1471-2121/10/65. Accessed 7 Oct 2009

  • Benhamed S, Guardiola FA, Mars M, Esteban MA (2014) Pathogen bacteria adhesion to skin mucus of fishes. Vet Microbiol 171:1–12. doi:10.1016/j.vetmic.2014.03.008

    Article  CAS  Google Scholar 

  • Benn T, Cavanagh B, Hristovski K, Posner JD, Westerhoff P (2010) The release of nanosilver from consumer products used in the home. J Environ Qual 39:1875–1882. doi:10.2134/jeq2009.0363

    Article  CAS  Google Scholar 

  • Bernadsky G, Rosenberg E (1992) Drag-reducing properties of bacteria from the skin mucus of the cornetfish (Fistularia commersonii). Microb Ecol 24(1):63–76. doi:10.1007/BF00171971

    Article  CAS  Google Scholar 

  • Bilberg K, Malte H, Wang T, Baatrup E (2010) Silver nanoparticles and silver nitrate cause respiratory stress in Eurasian perch (Perca fluviatilis). Aquat Toxicol 96:159–165. doi:10.1016/j.aquatox.2009.10.019

    Article  CAS  Google Scholar 

  • Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2012) In vivo toxicity of silver nanoparticles and silver ions in zebrafish (Danio rerio). J Toxicol 293784:9. doi:10.1155/2012/293784

    Google Scholar 

  • 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. doi:10.1016/j.scitotenv.2007.10.010

    Article  CAS  Google Scholar 

  • Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB (2009) Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94:320–327. doi:10.1016/j.aquatox.2009.07.019

    Article  CAS  Google Scholar 

  • Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu D-Y (2010) Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 100:151–159. doi:10.1016/j.aquatox.2009.12.012

    Article  CAS  Google Scholar 

  • Cordeiro LF, Marques BF, Wilges Kist L, Reis Bogo M, López G, Pagano G, Külkamp-Guerreiro IC, Monserrat JM (2014) Toxicity of fullerene and nanosilver nanomaterials against bacteria associated to the body surface of the estuarine worm Laeonereis acuta (Polychaeta, Nereididae). Mar Environ Res 99:52–59. doi:10.1016/j.marenvres.2014.05.011

    Article  CAS  Google Scholar 

  • Da Rocha AM, Salomão de Freitas DP, Burns M, Vieira JP, de la Torre FR, Monserrat JM (2009) Seasonal and organ variations in antioxidant capacity, detoxifying competence and oxidative damage in freshwater and estuarine fishes from Southern Brazil. Comp Biochem Physiol C 150:512–520. doi:10.1016/j.cbpc.2009.07.012

    Google Scholar 

  • Eduok S, Martin B, Villa R, Nocker A, Jefferson B, Coulon F (2013) Evaluation of engineered nanoparticle toxic effect on waste water microorganisms: current status and challenges. Ecotoxicol Environ Saf 95:1–9. doi:10.1016/j.ecoenv.2013.05.022

    Article  CAS  Google Scholar 

  • Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290. doi:10.1021/es803259g

    Article  CAS  Google Scholar 

  • Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531. doi:10.1016/j.envint.2010.10.012

    Article  CAS  Google Scholar 

  • Gagné F, André C, Skirrow R, Gélinas M, Auclair J, van Aggelen G, Turcotte P, Gagnon C (2012) Toxicity of silver nanoparticles to rainbow trout: a toxicogenomic approach. Chemosphere 89:615–622. doi:10.1016/j.chemosphere.2012.05.063

    Article  Google Scholar 

  • Gallagher EP, Canada AT, Di Giulio RT (1992) The protective role of glutathione in chlorothalonil-induced toxicity to channel catfish. Aquat Toxicol 23:155–168. doi:10.1016/0166-445X(92)90049-S

    Article  CAS  Google Scholar 

  • Garcia-Reyero N, Thornton C, Hawkins AD, Escalon L, Kennedy AJ, Steevens JA, Willett KL (2015) Assessing the exposure to nanosilver and silver nitrate on fathead minnow gill gene expression and mucus production. Environ Nanotechnol Monit Manag 4:58–66. doi:10.1016/j.enmm.2015.06.001

    Article  Google Scholar 

  • Geranio L, Heuberger M, Nowack B (2009) The behavior of silver nanotextiles during washing. Environ Sci Technol 43:8113–8118. doi:10.1021/es9018332

    Article  CAS  Google Scholar 

  • Griffitt RJ, Luo J, Gao J, Bonzongo J-C, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978. doi:10.1897/08-002.1

    Article  CAS  Google Scholar 

  • 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(2):404–415. doi:10.1093/toxsci/kfn256

    Article  CAS  Google Scholar 

  • Griffitt RJ, Lavelle CM, Kane AS, Denslow ND, Barber DS (2013) Chronic nanoparticulate silver exposure results in tissue accumulation and transcriptomic changes in zebrafish. Aquat Toxicol 130–131:192–200. doi:10.1016/j.aquatox.2013.01.010

    Article  Google Scholar 

  • Handy RD, von der Kammer F, Lead JR, Hassellöv M, Owen R, Crane M (2008) The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 17:287–314. doi:10.1007/s10646-008-0199

    Article  CAS  Google Scholar 

  • Hawkins AD, Thornton C, Steevens JA, Willett KL (2014) Alteration in Pimephales promelas mucus production after exposure to nanosilver or silver nitrate. Environ Toxicol Chem 33:2869–2872. doi:10.1002/etc.2759

    Article  CAS  Google Scholar 

  • Jovanović B, Palić D (2012) Immunotoxicology of non-functionalized engineered nanoparticles in aquatic organisms with special emphasis on fish—Review of current knowledge, gap identification, and call for further research. Aquat Toxicol 118–119:141–151. doi:10.1016/j.aquatox.2012.04.005

    Article  Google Scholar 

  • Katuli KK, Massarsky A, Hadadi A, Pourmehran Z (2014) Silver nanoparticles inhibit the gill Na +/K + -ATPase and erythrocyte AChE activities and induce the stress response in adult zebrafish (Danio rerio). Ecotoxicol Environ Saf 106:173–180. doi:10.1016/j.ecoenv.2014.04.001

    Article  CAS  Google Scholar 

  • Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3:95–101. doi:10.1016/j.nano.2006.12.001

    Article  CAS  Google Scholar 

  • Künniger T, Gerecke AC, Ulrich A, Huch A, Vonbank R, Heeb M, Wichser A, Haag R, Kunz P, Faller M (2014) Release and environmental impact of silver nanoparticles and conventional organic biocides from coated wooden façades. Environ Pollut 184:464–471. doi:10.1016/j.envpol.2013.09.030

    Article  Google Scholar 

  • Li WR, Xie XB, Shi QS, Zeng HY, You-Sheng OY, Chen YB (2010) Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl Microbiol Biotechnol 85:1115–1122. doi:10.1007/s00253-009-2159-5

    Article  CAS  Google Scholar 

  • Lorenz C, Windler L, von Goetz N, Lehmann RP, Schuppler M, Hungerbühler K, Heuberger M, Nowack B (2012) Characterization of silver release from commercially available functional (nano) textiles. Chemosphere 89:817–824. doi:10.1016/j.chemosphere.2012.04.063

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/s11051-010-9900-y

    Article  CAS  Google Scholar 

  • Marques BF, Cordeiro LF, Wilges Kist L, Reis Bogo M, López G, Pagano G, Tomazi Muratt D, de Carvalho LM, Külkamp-Guerreiro IC, Monserrat JM (2013) Toxicological effects induced by the nanomaterials fullerene and nanosilver in the polychaeta Laeonereis acuta (Nereididae) and in the bacteria communities living at their surface. Mar Environ Res 89:53–62. doi:10.1016/j.marenvres.2013.05.002

    Article  CAS  Google Scholar 

  • Massarsky A, Dupuis L, Taylor J, Eisa-Beygi S, Strek L, Trudeau VL, Moon TW (2013) Assessment of nanosilver toxicity during zebrafish (Danio rerio) development. Chemosphere 92:59–66. doi:10.1016/j.chemosphere.2013.02.060

    Article  CAS  Google Scholar 

  • Massarsky A, Trudeau VL, Moon TW (2014a) Predicting the environmental impact of nanosilver. Environ Toxicol Pharmacol 38:861–873. doi:10.1016/j.etap.2014.10.006

    Article  CAS  Google Scholar 

  • Massarsky A, Abraham R, Nguyen KC, Rippstein P, Tayabali AF, Trudeau VL, Moon TW (2014b) Nanosilver cytotoxicity in rainbow trout (Oncorhynchus mykiss) erythrocytes and hepatocytes. Comp Biochem Physiol C 159:10–21. doi:10.1016/j.cbpc.2013.09.008

    CAS  Google Scholar 

  • McNeil PL, Boyle D, Henry TB, Handy RD, Sloman KA (2014) Effects of metal nanoparticles on the lateral line system and behaviour in early life stages of zebrafish (Danio rerio). Aquat Toxicol 152:318–323. doi:10.1016/j.aquatox.2014.04.022

    Article  CAS  Google Scholar 

  • Merrifield DL, Shaw BJ, Harper GM, Saoud IP, Davies SJ, Handy RD, Henry TB (2013) Ingestion of metal-nanoparticle contaminated food disrupts endogenous microbiota in zebrafish (Danio rerio). Environ Pollut 174:157–163. doi:10.1016/j.envpol.2012.11.017

    Article  CAS  Google Scholar 

  • Messaoud M, Chadeau E, Brunon C, Ballet T, Rappenne L, Roussel F, Leonard D, Oulahal N, Langlet M (2010) Photocatalytic generation of silver nanoparticles and application to the antibacterial functionalization of textile fabrics. J Photochem Photobiol A215:147–156. doi:10.1016/j.jphotochem.2010.08.003

    Article  Google Scholar 

  • Neal AL (2008) What can be inferred from bacterium–nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles? Ecotoxicology 17:362–371. doi:10.1007/s10646-008-0217-x

    Article  CAS  Google Scholar 

  • Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627. doi:10.1126/science.1114397

    Article  CAS  Google Scholar 

  • Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463. doi:10.1016/S0166-445X(02)00204-7

    Article  CAS  Google Scholar 

  • Rather MA, Sharma R, Aklakur M, Ahmad S, Kumar N, Khan M, Ramya VL (2011) Nanotechnology: a novel tool for aquaculture and fisheries development. A prospective mini-review. Fish Aquac J 2011: FAJ-16 http://astonjournals.com/faj. Accessed 5 April 2011

  • Rhim J-W, Park H-M, Ha C-S (2013) Bio-nanocomposites for food packaging applications. Prog Polym Sci 38:1629–1652. doi:10.1016/j.progpolymsci.2013.05.008

    Article  CAS  Google Scholar 

  • Sakhtianchi R, Minchin RF, Ki-BumLee Alkilany AM, Serpooshan V, Mahmoudi M (2013) Exocytosis of nanoparticles from cells: role in cellular retention and toxicity. Adv Colloid Interface Sci 201–202:18–29. doi:10.1016/j.cis.2013.10.013

    Article  Google Scholar 

  • Scown TM, Santos EM, Johnston BD, Gaiser B, Baalousha M, Mitov S, Lead JR, Stone V, Fernandes TF, Jepson M, van Aerle R, Tyler CR (2010) Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol Sci 115(2):521–534. doi:10.1093/toxsci/kfq076

    Article  CAS  Google Scholar 

  • Shaw BJ, Handy RD (2011) Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environ Int 37(6):1083–1097. doi:10.1016/j.envint.2011.03.009

    Article  CAS  Google Scholar 

  • Shrivastava S, Bera T, Roy A, Singh G, Ramachandrarao P, Dash D (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18:225103. doi:10.1088/0957-4484/18/22/225103

    Article  Google Scholar 

  • Soltani M, Ghodratnema M, Ahari H, Ebrahimzadeh Mousavi HA, Atee M, Dastmalchi F, Rahmanya J (2009) The inhibitory effect of silver nanoparticles on the bacterial fish pathogens, Streptococcus iniae, Lactococcus garvieae, Yersinia ruckeri and Aeromonas hydrophila. Int J Vet Res 3(2):137–142

    Google Scholar 

  • Taju G, Abdul Majeed S, Nambi KSN, Sahul Hameed AS (2014) In vitro assay for the toxicity of silver nanoparticles using heart and gill cell lines of Catla catla and gill cell line of Labeo rohita. Comp Biochem Physiol C 161:41–52. doi:10.1016/j.cbpc.2014.01.007

    CAS  Google Scholar 

  • Tiede K, Hassellöv M, Breitbarth E, Chaudhry Q, Boxall ABA (2009) Considerations for environmental fate and ecotoxicity testing to support environmental risk assessments for engineered nanoparticles. J Chromatogr A 1216:503–509. doi:10.1016/j.chroma.2008.09.008

    Article  CAS  Google Scholar 

  • Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, Roszek B, Bisschops J, Gosens I, van de Meent D, Dekkers S, de Jong WH, van Zijverden M, Sips AJAM, Geertsma RE (2009) Nano-silver: a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3(2):109–138. doi:10.1080/17435390902725914

    Article  CAS  Google Scholar 

  • Wilson B, Danilowicz BS, Meijer WG (2008) The diversity of bacterial communities associated with atlantic cod Gadus morhua. Microb Ecol 55:425–434. doi:10.1007/s00248-007-9288-0

    Article  Google Scholar 

  • Wu Y, Zhou Q (2012) Dose- and time-related changes in aerobic metabolism, chorionic disruption, and oxidative stress in embryonic medaka (Oryzias latipes): underlying mechanisms for silver nanoparticle developmental toxicity. Aquat Toxicol 124–125:238–246. doi:10.1016/j.aquatox.2012.08.009

    Article  Google Scholar 

  • Wu Y, Zhou Q (2013) Silver nanoparticles cause oxidative damage and histological changes in medaka (Oryzias latipes) after 14 days of exposure. Environ Toxicol Chem 32(1):165–173. doi:10.1002/etc.2038

    Article  CAS  Google Scholar 

  • Zhao J, Wang Z, Liu X, Xie X, Zhang K, Xing B (2011) Distribution of CuO nanoparticles in juvenile carp (Cyprinus carpio) and their potential toxicity. J Hazard Mater 197:304–310. doi:10.1016/j.jhazmat.2011.09.094

    Article  CAS  Google Scholar 

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Acknowledgments

L. Machado de Carvalho and J.M.Monserrat are research fellows from Brazilian CNPq. The work was supported by Nanotoxicology Network (MCTI/CNPq Process Number 552131/2011-3).

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Correspondence to Carla Bacchetta.

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Bacchetta, C., López, G., Pagano, G. et al. Toxicological Effects Induced by Silver Nanoparticles in Zebra Fish (Danio Rerio) and in the Bacteria Communities Living at Their Surface. Bull Environ Contam Toxicol 97, 456–462 (2016). https://doi.org/10.1007/s00128-016-1883-7

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