Abstract
This work addressed the trophic transfer and effects of functionalized gold nanoparticles (AuNPs) from periphytic biofilms to the crustacean Gammarus fossarum. Biofilms were exposed for 48 h to 10 nm positively charged functionalized AuNPs at two concentrations, 4.6 and 46 mg/L, and crustaceans G. fossarum grazed on these for 7 days, with daily biofilm renewal. Gold bioaccumulation in biofilm and crustacean were measured to estimate the trophic transfer ratio of these AuNP, and, for the first time, a transcriptomic approach and transmission electron microscopy observations in the crustacean were made. These two approaches showed cellular damage caused by oxidative stress and, in particular, an impact of these AuNPs on mitochondrial respiration. Modulation of digestive enzyme activity was also observed, suggesting modifications of digestive functions. The damage due to these nanoparticles could then have vital consequences for the organisms during chronic exposure.
Similar content being viewed by others
References
Abreu PC, Ballester ELC, Odebrecht C, Wasielesky W Jr, Cavalli R, Granéli W (2007) Importance of biofilm as food source for shrimp (Farfantepenaeus paulensis) evaluated by stable isotopes (δ13C and δ15N). J Exp Mar Biol Ecol 347:88–96
Achard M, Baudrimont M, Boudou A, Bourdineaud JP (2004) Induction of a multixenobiotic resistance protein (MXR) in the Asiatic clam Corbicula fluminea after heavy metals exposure. Aquat Toxicol 67:347–357
Adam O (2008) Impact des produits de traitement du bois sur les amphipodes Gamamrus pulex (L.) et Gammarus fossarum (K.) : approches chimiques, hydro-écologique et écotoxicologique. PhD thesis, University of Franche-comté, France
Amiard J, Amiard-Triquet C, Barka 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
Andrei J, Pain-Devin S, Felten V, Devin S, Giambérini L, Mehennaoui K, Cambier S, Gutleb AC, Guérold F (2016) Silver nanoparticles impact the functional role of Gammarus roeseli (Curstacea Amphipoda). Environ Pollut 208:608–618
Arini A, Feurtet-Mazel A, Morin S, Maury-Brachet R, Coste M, Delmas F (2012a) Remediation of a watershed contaminated by heavy metals: a 2-year field biomonitoring of periphytic biofilms. STOTEN 425:242–253
Arini A, Feurtet-Mazel A, Maury-Brachet R, Pokrovsky O, Coste M, Delmas F (2012b) Recovery potential of periphytic biofilms translocated in artificial streams after industrial contamination (Cd and Zn). Ecotoxicology 21:1403–1414
Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S, Brisson A (2014) Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thrombose Haemost 12:614–627
Aueviriyavit S, Phummiratch D, Maniratanachote R (2014) Mechanistic study on the biological effects of silver and gold nanoparticles in Caco-2 cells – induction of the Nrf2/HO-1 pathway by high concentrations of silver nanoparticles. Toxico Lett 224:73–83
Auffan M, Rose J, Wiesner MR, Bottero JY (2009) Chemical stability of metallic NPs: a parameter controlling their potential cellular toxicity in vitro. Environ Poll 157:1127–1133
Bajak E, Fabbri M, Ponti J, Gioria S, Ojea-Jimenez I, Collotta A, Mariani V, Gilliland D, Rossi F, Gribaldo L (2014) Changes in Caco-2 cells transcriptome profiles upon exposure to gold nanoparticles. Toxicol Lett doi. doi:10.1016/j.toxlet.2014.12.008
Baudrimont M, Andrès S, Durrieu G, Boudou A (2003) The key role of metallothioneins in the bivalve Corbicula fluminea during the depuration phase, after an in situ exposure to Cd and Zn. Aquat Toxicol 63:89–102
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Chatterjee A, Priyam A, Bhattacharya SC, Saha A (2007) pH dependent interaction of biofunctionalized CdS NPs with nucleobases and nucleotides: a fluorimetric study. J lumen 126:764–770
Chithrani BD, Ghazani AA, Chan WC (2006) Determining size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6:662–668
Connor E, Mwamuka J, Gole A, Murphy CJ, Wyatt MD (2005) Gold NPs are taken up by human cells but do not acute cytotoxicity. Small 1:325–327
Correia AD, Livingstone DR, Helena Costa M (2002) Effects of water-borne copper on metallothionein and lipid peroxidation in the marine amphipod Gammarus locusta. Mar Environ Res 54:357–360
Dauta A (1982) Conditions de développement du phytoplancton. Etude comparative du comportement de huit espèces en culture. Ann Limnol:217–262
Dedeh A, Ciutat A, Treguer-Delapierre M, Bourdineaud JP (2014) Impact of gold nanoparticles on zebrafish exposed to a spiked sediment. Nanotoxicology. doi:10.3109/17435390.2014.889238
Dedourge-Geffard O, Palais F, Biagianti-Risbourg S, Geffard O, Geffard A (2009) Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere 77:1569–1576
Duong TT, Morin S, Herlory O, Feurtet-Mazel A, Coste M, Boudou A (2008) Seasonal effects of cadmium accumulation in periphytic diatom communities of freshwater biofilms. Aquat Toxicol 90:19–28
Duong TT, Morin S, Coste M, Herlory O, Feurtet-Mazel A, Boudou A (2010) Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. STOTEN 408:552–562
Ernest V, Shiny PJ, Mukherjee A, Chandrasekaran N (2012) Silver nanoparticles: a potential nanocatalyst for the rapid degradation of starch hydrolysis by alpha-amylase. Carbohydrate Res 352:60–64
Farkas J, Christian P, Gallego Urrea JA, Roos N, Hassellöv M, Tollefsen KE, Thomas KV (2009) Effects of silver and gold nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 96:44–52
Fouqueray M, Dufils B, Vollat B, Chaurand P, Botta C, Abacci K, Labille J, Rose J, Garric J (2012) Effects of aged TiO2 nanomaterial from sunscreen on Daphnia magna exposed by dietary route. Environ Poll 163:55–61
Garcia-carreño FL, Haard N (1993) Characterization of proteinase classes in langostilla (Pleuroncodes planipes) and crayfish (Pacifastacus astacus) extracts. J Food Biochem 17:97–113
Hochepied JF and Guyot-Ferréol V (2007) Cosmétique et nanomatériaux. www.ep.ensmp.fr/scpi/PubliSCPI/nanocosmetique.pdf
Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V (2010) A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 40:328–346
Kelly DW, Dick JTA, Montgomery WI (2002) The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators, or both? Hydrobiologia 485:199–203
Kim J, Piao Y, Hyeon T (2009) Multifunctional nanostructured materials for multimodal imaging, and simultaneous imaging and therapy. Chem Soc Rev 38:372–390
Koehler A, Marx U, Broeg K, Bahns S, Bressling J (2010) Effects of nanoparticles in Mytilus edulis gills and hepatopancreas a new threat to marine life? Mar Environ Res 66:12–14
Lacaze E (2011) Un biomarqueur de génotoxicité chez Gammarus fossarum : développement, signification fonctionnelle et application au milieu naturel. Ph.D. Thesis, University of Metz
Lebrun JD, Perret M, Geffard A, Gourlay-Francé C (2012) Modelling copper bioaccumulation in Gammarus pulex and alterations of digestive metabolism. Ecotoxicology 21:2022–2030
Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–49
Livak J, Schmittgen TT (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (−Delta Delta C(T)) method., in. Methods 25:402–408
Mehennaoui K, Georgantzopoulou A, Felten V, Andrei J, Garaud M, Cambier S, Serchi T, Pain-Devin S, Guérold F, Audinot J-N, Giambérini L, Gutleb A (2016) Gammarus fossarum (crustacean, Amphipoda) as a model organism to study the effects of silver nanoparticles. STOTEN 566-567:1649–1659
Morin S, Duong TT, Herlory O, Feurtet-Mazel A, Coste M (2008) Cadmium toxicity and bioaccumulation in freshwater biofilms. Arch Environ Contam Toxicol 54:173–186
Muralisankar T, Bhavan PS, Radhakrishnan S, Manickam N, Srinivasan V (2014) Dietary supplementation of zinc nanoparticles and its influence on biology, physiology and immune responses of the freshwater prawn, Macrobrachium rosenbergii. Biol Trace Elem Res 160:56–66
Palais F, Jubeaux G, Dedourge-Geffard O, Biagianti-Risbourg S, Geffard A (2010) Amylolytic and cellulolytic activities in the crystalline style and the digestive diverticulae of the freshwater bivalve Dreissena polymorpha (Pallas,1771). Molluscan Res 30:29–36
Paul-Pont I, de Montaudouin X, Gonzalez P, Jude F, Raymond N, Paillard C, Baudrimont M (2010) Interactive effects of metal contamination and pathogenic organisms on the introduced marine bivalve Ruditapes philippinarum in European populations. Environ Poll 158:3401–3410
Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R (2007) Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2:751–760
Renault S, Baudrimont M, Mesmer-Dudons N, Gonzalez P, Mornet S, Brisson A (2008) Impacts of gold nanoparticle exposure on two freshwater species: a phytoplanktonic alga (Scenedesmus subspicatus) and a benthic bivalve (Corbicula fluminea). Gold Bull 41:116–126
Rothen-Rutishauser BM, Schürch S, Haenni B, Kappa N, Gehr P (2006) Interaction of fine particles and NPs with red blood cells visualized with advanced microscopic technique. ES&T 40:4353–4359
Russell R and Cresanti R (2006) Environmental, Health, and Safety research needs for engineering nanoscale materials. Nanoscale science, engineering, and technology subcommittee
Schmitz G, Minkel DT, Gingrich D, Shaw CF III (1980) The binding of gold (I) to metallothionein. J Inorg Biochem 293–230
Schrand AM, Rahman MF, Hussain SM, Schlager JJ, Smith DA, Syed AF (2010) Metal-based nanoparticles and their toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:544–568
Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde RR, Sastry M (2005) Biocompatibility of gold NPs and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir 21:10644–10654
Yu S, Rui Q, Cai T, Wu Q, Li Y, Wang D (2011) Close association of intestinal autofluorescence with the formation of severe oxidative damage in, intestine of nematodes chronically exposed to Al2O3-nanoparticle. Environ Toxicol Pharmacol 32:233–241
Acknowledgements
The authors thank the Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail (ANSES) research program TRONANO, for their support of this work. They also thank Bruno Etcheverria from the EPOC laboratory (University of Bordeaux) for his support in laboratory work, and the Bordeaux Imaging Center which allowed us access to their microscopic devices. This work was also supported by the Agence Nationale de la Recherche (ANR) in the CITTOXIC-Nano program (ANR-14-CE21-0001-01) and the Investments for the future Program, within the Cluster of Excellence COTE (ANR-10-LABX-45).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Baudrimont, M., Andrei, J., Mornet, S. et al. Trophic transfer and effects of gold nanoparticles (AuNPs) in Gammarus fossarum from contaminated periphytic biofilm. Environ Sci Pollut Res 25, 11181–11191 (2018). https://doi.org/10.1007/s11356-017-8400-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-8400-3