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Original Article

Digestive cell lysosomes as main targets for Ag accumulation and toxicity in marine mussels, Mytilus galloprovincialis, exposed to maltose-stabilised Ag nanoparticles of different sizes

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Pages 168-183 | Received 06 Jun 2016, Accepted 13 Dec 2016, Published online: 24 Jan 2017

References

  • Abbe GR, Sanders JG. 1990. Pathways of silver uptake and accumulation by the American oyster (Crassostrea virginica) in Chesapeake Bay. Estuar Coast Shelf Sci 31:113–23.
  • Abbe GR, Sanders J, Riedel GF. 1994. Silver Uptake by the oyster (Crassostrea virginica): effect of organism size and storage sites. Estuar Coast Shelf Sci 39:249–60.
  • Amiard JC, Amiard-Triquet C, Barla S, Pellerin J, Rainbow PS. 2006. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202.
  • Asharani P V, Wu YL, Gong Z, Valiyaveettil S. 2008. Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19:2255102–107.
  • Asharani PV, Kah Mun GL, Prakash Hande M, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–90.
  • Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY. 2009. Toxicity assessment of multisized gold and silver nanoparticles in zebrafish embryos. Small 5:1897–910.
  • Batchelor-McAuley C, Tschulik K, Neumann CCM, Laborda E, Compton RG. 2014. Why are silver nanoparticles more toxic than bulk silver? Towards understanding the dissolution and toxicity of silver nanoparticles. Int J Electrochem Sci 9:1132–8.
  • Behra R, Sigg L, Clift MJD, Herzog F, Minghetti M, Johnston B, et al. 2013. Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J R Soc Interface 10:20130396. doi:10.1098/rsif.2013.0396.
  • Benn TM, Westerhoff P. 2008. Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–9.
  • Bianchini A, Grosell M, Gregory SM, Wood CM. 2002. Acute silver toxicity in aquatic animals is a function of sodium uptake rate. Environ Sci Technol 36:1763–6.
  • Bilberg K, Malte H, Wang T, Baatrup E. 2010. Silver nanoparticles and silver nitrate cause respiratory stress in Eurasian perch (Perca fluviatilis). Aquat Toxicol 96:159–65.
  • Boenigk J, Beisser D, Zimmermann S, Bock C, Jakobi J, Grabner D, et al. 2014. Effects of silver nitrate and silver nanoparticles on a planktonic community: general trends after short-term exposure. PLoS One 9:e95340. doi:10.1371/journal.pone.0095340
  • Boya P, Kroemer G. 2008. Lysosomal membrane permeabilization in cell death. Oncogene 27:6434–51.
  • Buffet PE, Pan JF, Poirier L, Amiard-Triquet C, Amiard JC, Gaudin P, et al. 2013. Biochemical and behavioural responses of the endobenthic bivalve Scrobicularia plana to silver nanoparticles in seawater and microalgal food. Ecotox Environ Safety 89:117–24.
  • Buffet PE, Zalouk-Vergnoux A, Châtel A, Berthet B, Métais I, Perrein-Ettajani H, et al. 2014. A marine mesocosm study on the environmental fate of silver nanoparticles and toxicity effects on two endobenthic species: the ragworm Hediste diversicolor and the bivalve mollusc Scrobicularia plana. Sci Tot Environ 470–471:1151–9.
  • Bury NR, Wood CM. 1999. Mechanism of branchial apical silver uptake by rainbow trout is via the proton-coupled Na + channel. Am J Physiol 277:1385–91.
  • Bystrzejewska-Piotrowska G, Golimowski J, Urban PL. 2009. Nanoparticles: Their potential toxicity, waste and environmental management. Waste Manag 29:2587–95.
  • Cajaraville MP, Díez G, Marigómez IA, Angulo E. 1990. Responses of basophilic cells of the digestive gland of mussels to petroleum hydrocarbon exposure. Dis Aquat Organ 9:221–8.
  • Cajaraville MP, Abascal I, Etxeberria M, Marigómez I. 1995. Lysosomes as cellular markers of environmental pollution: time- and dose-dependent responses of the digestive lysosomal system of mussels after petroleum hydrocarbon exposure. Environ Toxicol Water Qual 10:1–8.
  • Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A. 2000. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311.
  • Calabrese A, Collier RS, Nelson DA, MacInnes JR. 1973. The toxicity of heavy metals to embryos of the American oyster Crassostrea virginica. Mar Biol 18:162–6.
  • Calabrese A, Nelson DA. 1974. Inhibition of embryonic development of the hard clam, Mercenaria mercenaria, by heavy metals. Bull Environ Contam Toxicol 11:92–7.
  • Canesi L, Ciacci C, Fabbri R, Marcomini A, Pojana G, Gallo G. 2012. Bivalve molluscs as a unique target group for nanoparticle toxicity. Mar Environ Res 76:16–21.
  • Chiffoleau JF, Auger D, Roux N, Rozuel E, Santini A. 2005. Distribution of silver in mussels and oysters along the French coasts: data from the national monitoring program. Mar Pollut Bull 50:1719–23.
  • Cong Y, Banta GT, Selck H, Berhanu D, Valsami-Jones E, Forbes VE. 2014. Toxicity and bioaccumulation of sediment-associated silvernanoparticles in the estuarine polychaete, Nereis (Hediste) diversicolor. Aquat Toxicol 156:106–15.
  • Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, et al. 2013. Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 9:970–82.
  • Dai L, Banta GT, Selck H, Forbes VE. 2013. Effects, uptake, and depuration Kinetics of silver oxide and copper oxide nanoparticles in a marine deposit feeder, Macoma balthica. ACS Sustainable Chem Eng 1:760–7.
  • Da Ros L, Nasci C, Marigómez I, Soto M. 2000. Biomarkers and trace metals in the digestive gland of indigenous and transplanted mussels, Mytilus galloprovincialis, in Venice Lagoon, Italy. Mar Environ Res 50:417–23.
  • Danscher G. 1981. Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Histochemistry 71:1–16.
  • Danscher G, Hacker G, Hauser-Kronberger C, Grimelius L. 1995. Trends in autometallographic silver amplification of colloidal gold particles. In: Hayat MA, ed. Immunogold Silver Staining: Principles, Methods and Applications. Boca Raton, FL: CRC Press Inc., 336.
  • Drake PL, Hazelwood KJ. 2005. Exposure-related health effects of silver and silver compounds: a review. Ann Occup Hyg 49:575–85.
  • Efron B, Tibshirani RJ. 1993. An Introduction to the Bootstrap. London: Chapman & Hall.
  • Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR. 2011. Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–31.
  • Fabrega J, Renshaw JC, Lead JR. 2009. Interactions of silver nanoparticles with Pseudomonas putida biofilms. Environ Sci Technol 43:9004–9.
  • Farkas J, Christian P, Urrea JAG, Roos N, Hassellöv M, Tollefsen KE, Thomas KV. 2010. Effects of silver and gold nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 96:44–52.
  • García-Alonso J, Khan FR, Misra SK, Turmaine M, Smith BD, Rainbow PS, et al. 2011. Cellular internalization of silver nano-particles in gut epithelia of the estuarine polychaete Nereis diversicolor. Environ Sci Technol 45:4630–6.
  • Garmendia L, Soto M, Vicario U, Kim Y, Cajaraville MP, Marigómez I. 2011. Application of a battery of biomarkers in mussel digestive gland in order to assess long-term effects of the Prestige oil spill in Galicia and Bay of Biscay: tissue-level biomarkers and histopathology. J Environ Monit 13:915–32.
  • George SG, Pirie BJS, Calabrese A, Nelson DA. 1986. Biochemical and ultrastructural observations of long-term silver accumulation in the mussel, Mytilus edulis. Mar Environ Res 18:255–65.
  • Gliga AR, Skoglund S, Wallinder IO, Fadeel b, Karlsson HL. 2014. Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol 11:11. doi:10.1186/1743-8977-11-11.
  • Glover RD, Miller JM, Hutchison JE. 2011. Generation of metal nanoparticles from silver and copper objects: nanoparticle dynamics on surfaces and potential sources of nanoparticles in the environment. Acs Nano 5:8950–7.
  • Gomes T, Araújo O, Pereira R, Almeida AC, Cravo A, Bebianno MJ. 2013a. Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis. Mar Environ Res 84:51–9.
  • Gomes T, Pereira CG, Cardoso C, Bebianno MJ. 2013b. Differential protein expression in mussels Mytilus galloprovincialis exposed to nano and ionic Ag. Aquat Toxicol 136–137:79–90.
  • Gottschalk F, Sonderer T, Scholz RW, Nowack B. 2009. Modelled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–22.
  • Griffitt RJ, Brown-Peterson NJ, Savin DA, Manning CS, Boube I, Ryan RA, Brouwer M. 2012. Effects of chronic nanoparticulate silver exposure to adult and juvenile sheepshead minnows (Cyprinodon variegatus). Environ Toxicol Chem 31:160–7.
  • Hackenberg S, Scherzed A, Kessler M, Hummel S, Technau A, Froelich K, et al. 2011. Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol Lett 201:27–33.
  • Handy RD, Cornelis G, Fernandes T, Tsyusko O, Decho A, Sabo-Attwood T, et al. 2012. Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environ Toxicol Chem 31:15–31.
  • Hartmann NB, Baun A. 2010. The nano cocktail: ecotoxicological effects of engineered nanoparticles in chemical mixtures. Integr Environ Assess Manag 6:311–14.
  • Hayat MA. 2000. Principles and Techniques of Electron Microscopy: Biological Applications. Cambridge: Cambridge University Press.
  • Hull MS, Vikesland PJ, Schultz IR. 2013. Uptake and retention of metallic nanoparticles in the Mediterranean mussel (Mytilus galloprovincialis). Aquat Toxicol 140–141:89–97.
  • Jimeno-Romero A, Oron M, Cajaraville MP, Soto M, Marigómez I. 2016. Nanoparticle size and combined toxicity of TiO2 and DSLS (surfactant) contribute to lysosomal responses in digestive cells of mussels exposed to TiO2 nanoparticles. Nanotoxicology 10:1168–76.
  • Johnston BD, Scown TM, Moger J, Cumberland SA, Baalousha M, Linge K, et al. 2010. Bioavailability of nanoscale metal oxides TiO(2), CeO(2), and ZnO to fish. Environ Sci Technol 44:1144–51.
  • Kaegi R, Sinnet B, Zuleeg S, Hagendorfer H, Mueller E, Vonbank R, et al. 2010. Release of silver nanoparticles from outdoor facades. Environ Pollut 158:2900–5.
  • Katsumiti A, Gilliland D, Arostegui I, Cajaraville MP. 2015. Mechanisms of toxicity of Ag nanoparticles in comparison to bulk and ionic Ag on mussel hemocytes and gill cells. PLoS One 10:e0129039. doi:10.1371/journal.pone.0129039.
  • Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY. 2009. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro 23:1076–84.
  • Koehler A, Marx U, Broeg K, Bahns S, Bressling J. 2008. Effects of nanoparticles in Mytilus edulis gills and hepatopancreas – a new threat to marine life? Mar Environ Res 66:12–4.
  • Kroemer G, Jäättelä M. 2005. Lysosomes and autophagy in cell death control. Nat Rev Cancer 5:886–97.
  • Kvitek L, Prucek R, Panáček A, Novotny R, Hrbac J, Zbořil R. 2005. The influence of complexing agent concentration on particle size in the process of SERS active silver colloid synthesis. J Mater Chem 15:1099–105.
  • Kvitek L, Vanickova M, Panacek A, Soukupova J, Dittrich M, Valentova E, et al. 2009. Initial study on the toxicity of silver nanoparticles (nps) against Paramecium caudatum. J Phys Chem C 113:4296–300.
  • Lanceleur L, Schafer J, Bossy C, Coynel A, Larosse A, Masson M, Blanc G. 2011. Silver fluxes to the Gironde Estuary – Eleven years (1999–2009) of monitoring at the watershed scale. Appl Geochem 26:797–808.
  • Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, et al. 2007. Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–34.
  • Liu J, Hurt RH. 2010. Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–75.
  • Liu J, Sonshine DA, Shervani S, Hurt RH. 2010. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4:6903–13.
  • Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, et al. 2010. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 4:319–30.
  • Loeschner K, Hadrup N, Qvortrup K, Larsen A, Gao X, Vogel U, et al. 2011. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 8:18.
  • Luoma SN. 2008. Silver Nanotechnologies and the Environment: Old Problems or New Challenges? Project on Emerging Nanotechnologies. Publication 15. Washington, DC: Woodrow Wilson International Center for Scholars and PEW charitable Trusts.
  • Luoma SN, Ho YB, Bryan GW. 1995. Fate, bioavailability and toxicity of silver in estuarine environments. Mar Pollut Bull 131:44–54.
  • Luther EM, Koehler Y, Diendorf J, Epple M, Dringen R. 2011. Accumulation of silver nanoparticles by cultured primary brain astrocytes. Nanotechnology 22:375101–11.
  • Mackay EA, Overnell J, Dunbar B, Davidson I, Hunziker PE, Kagi JHR, Fothergill JE. 1993. Complete amino acid sequences of five dimeric and four monomeric forms of metallothionein from the edible mussel Mytilus edulis. Eur J Biochem 218:183–94.
  • Manno D, Serra A, Buccolieri A, Panzarini E, Carata E, Tenuzzo B, et al. 2013. Silver and carbon nanoparticles toxicity in sea urchin Paracentrotus lividus embryos. BioNanoMaterials 14:229–38.
  • Marigómez IA, Cajaraville MP, Angulo E, Moya J. 1990. Ultrastructural alterations in the renal epithelium of cadmium- treated Littorina littorea (L.). Arch Environ Contam Toxicol 19:863–71.
  • Marigómez I, Soto M, Cajaraville MP, Angulo E, Giamberini L. 2002. Cellular and subcellular distribution of metals in molluscs. Microsc Res Tech 50:358–92.
  • Marigómez I, Soto M, Cancio I, Orbea A, Garmendia L, Cajaraville MP. 2006. Cell and tissue biomarkers in mussel, and histopathology in hake and anchovy from Bay of Biscay after the Prestige oil spill (Monitoring Campaign 2003). Mar Pollut Bull 53:287–304.
  • Marigómez I, Garmendia L, Soto M, Orbea A, Izagirre U, Cajaraville MP. 2013a. Marine ecosystem health status assessment through integrative biomarker indices: a comparative study after the Prestige oil spill "Mussel Watch". Ecotoxicology 22:486–505.
  • Marigómez I, Zorita I, Izagirre U, Ortiz-Zarragoitia M, Navarro P, Etxebarria N, et al. 2013b. Combined use of native and caged mussels to assess biological effects of pollution through the integrative biomarker approach. Aquat Toxicol 136/137:32–48.
  • Martoja R, Ballan-Dufrançais C, Jeantet AY, Gsuzerh P, Amiard C, Amiard-Triquet C, et al. 1988. Effets chimiques et cytologiques de la contamination expérimentale de l'huitre Crassostrea gigas Thunberg par l'argent administre sous forme dissoute et par voie alimentaire. Can J Fish Aquat Sci 45:1827–44.
  • 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.
  • Meyer JN, Lord CA, Yang XY, Turner EA, Badireddy AR, Marinakos SM, et al. 2010. Intracellular uptake and associated toxicity of silver nanoparticles in Caenorhabditis elegans. Aquat Toxicol 100:140–50.
  • Mikolaczyk M, Rementeria A, Lanceleur L, Schafer J, Petit JC, Zaldibar B, et al. 2015. Silver and copper bioaccumulation kinetics in oyster Crassostrea gigas tissues at environmentally relevant exposure levels using stable isotope spikes. Estuar Coast Shelf Sci 179:135–44.
  • Milić M, Leitinger Pavičić I, Avdičević MZ, Dobrović S, Goessler W, Vrček IV. 2015. Cellular uptake and toxicity effects of silver nanoparticles in mammalian kidney cells. J Appl Toxicol 35:581–92.
  • Montes MO, Hanna SK, Lenihan HS, Keller AA. 2012. Uptake, accumulation, and biotransformation of metal oxide nanoparticles by a marine suspension-feeder. J Hazard Mater 225–226:139–45.
  • Moore MN. 1990. Lysosomal cytochemistry in marine environmental monitoring. Histochem J 22:189–91.
  • Moore MN. 2006. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–76.
  • Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ. 2005. The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–53.
  • Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, et al. 2008. Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–64.
  • Nelson DA, Calabrese A, Greig RA, Yevich PP, Chang S. 1983. Long-term silver effects on the marine gastropod Crepidula fornicata. Mar Ecol Prog Ser 12:155–65.
  • Park E-J, Yi J, Kim Y, Choi K, Park K. 2010. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro 24:872–8.
  • Porte C, Sole M, Borghi V, Martinez M, Chamorro J, Torreblanca A, et al. 2001. Chemical, biochemical and cellular responses in the digestive gland of the mussel Mytilus galloprovincialis from the Spanish Mediterranean coast. Biomarkers 6:335–50.
  • Ramskov T, Forbes VE, Gilliland D, Selck H. 2015. Accumulation and effects of sediment-associated silver nanoparticles to sediment-dwelling invertebrates. Aquat Toxicol 166:96–105.
  • Ringwood AH, McCarthy M, Bates TC, Carroll DL. 2010. The effects of silver nanoparticles on oyster embryos. Mar Environ Res 69:49–51.
  • Scown TM, Santos EM, Johnston BD, Gaiser B, Baalousha M, Mitov S, et al. 2010. Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol Sci 115:521–34.
  • Singh RP, Ramarao P. 2012. Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles. Toxicol Lett 213:249–59.
  • 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 275:177–82.
  • Soto M, Marigómez I. 1997. BSD extent, an index for metal pollution screening based on the metal content within digestive cell lysosomes of mussels as determined by autometallography. Ecotox Environ Safety 37:141–51.
  • Soto M, Zaldibar B, Cancio I, Taylor MG, Turner M, Morgan AJ, Marigómez I. 2002. Subcellular distribution of cadmium and its cellular ligands in mussel digestive gland cells as revealed by combined autometallography and X-ray microprobe analysis. Histochem J 34:273–80.
  • Stern S, Adiseshaiah P, Crist R. 2012. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol 9:20.
  • Tappin AD, Barriada JL, Braungardt CB, Evans H, Patey MD, Achterberg EP. 2010. Dissolved silver in European estuarine and coastal waters. Water Res 44:4204–16.
  • Tedesco S, Doyle H, Blasco J, Redmond G, Sheehan D. 2010. Exposure of the blue mussel, Mytilus edulis, to gold nanoparticles and the pro-oxidant menadione. Comp Biochem Physiol C Toxicol Pharmacol 151:167–74.
  • Tupling R, Green H. 2002. Silver ions induce Ca2+ release from the SR in vitro by acting on the Ca2+ release channel and the Ca2+ pump. J Appl Physiol 92:1603–10.
  • UNEP/RAMOGE. 1999. Manual on the Biomarkers Recommended for the MED POL Biomonitoring Programme. Athens: UNEP.
  • Wang H, Wu L, Reinhard BM. 2012. Scavenger receptor mediated endocytosis of silver nanoparticles into J774A.1 macrophages is heterogeneous. ACS Nano 6:7122–32.
  • Yamashima T, Oikawa S. 2009. The role of lysosomal rupture in neuronal death. Prog Neurobiol 89:343–58.
  • Yang XY, Gondikas AP, Marinakos SM, Auffan M, Liu J, Hsu-Kim H, Meyer JN. 2012. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol 46:1119–27.
  • Yu SJ, Chao JB, Sun J, Yin YG, Liu JF, Jiang GB. 2013. Quantification of the uptake of silver nanoparticles and ions to HepG2 cells. Environ Sci Technol 47:3268–74.
  • Zaldibar B, Cancio I, Marigómez I. 2007. Reversible alterations in epithelial cell turnover in digestive gland of winkles (Littorina littorea) exposed to cadmium and their implications for biomarker measurements. Aquat Toxicol 81:183–96.
  • Zhao F, Zhao Y, Liu Y, Chang X, Chen C, Zhao YZ. 2011. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small 7:1322–37.
  • Zorita I, Ortiz-Zarragoitia M, Soto M, Cajaraville MP. 2006. Biomarkers in mussels from a copper site gradient (Visnes, Norway): an integrated biochemical, histochemical and histological study. Aquat Toxicol 78:109–16.
  • Zorita I, Bilbao E, Schad A, Cancio I, Soto M, Cajaraville MP. 2007. Tissue- and cell-specific expression of metallothionein genes in cadmium- and copper-exposed mussels analyzed by in situ hybridization and RT–PCR. Toxicol Appl Pharmacol 220:186–96.
  • Zuykov M, Pelletier E, Demers S. 2011. Colloidal complexed silver and silver nanoparticles in extrapallial fluid of Mytilus edulis. Mar Environ Res 71:17–21.

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