Skip to main content
SpringerLink
Log in

Silver nanoparticles impact phototrophic biofilm communities to a considerably higher degree than ionic silver

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Due to the significant increase in nanoparticle production and especially that of silver nanoparticles over the past decade, the toxicity of silver in both ionic (Ag+) and nanoparticulate (AgNPs) form must be studied in detail in order to understand their impact on natural ecosystems. A comparative study of the effect of AgNPs and ionic silver on two independent phototrophic biofilms was conducted in a rotating annular bioreactor (RAB) operating under constant conditions. The concentration of dissolved silver in the inlet solution was progressively increased every 4 days of exposure, from 0.1 to 100 μg L−1. In the course of the 40-day experiment, biofilm samples were collected to determine the evolution of biomass, chlorophyll-a, as well as photosynthetic and heterotrophic enzymatic activities in response to silver addition. Analysis of both dissolved and particulate silver allowed quantification of the distribution coefficient and uptake rate constants. The presence of both AgNPs and Ag+ produced significant changes in the biofilm structure, decreasing the relative percentage of Diatomophyceae and Cyanophyceae and increasing the relative percentage of Chlorophyceae. The accumulation capacity of the phototrophic biofilm with respect to ionic silver and the corresponding distribution coefficients were an order of magnitude higher than those of the phototrophic biofilm with respect to AgNPs. Higher levels of AgNPs decreased the biomass from 8.6 ± 0.2 mg cm−2 for 0–10 μg L−1 AgNPs to 6.0 ± 0.1 mg cm−2 for 100 μg L−1 added AgNPs, whereas ionic silver did not have any toxic effect on the biofilm growth up to 100 μg L−1 of added Ag+. At the same time, AgNPs did not significantly affect the photosynthetic activity of the biofilm surface communities compared to Ag+. It can thus be hypothesized that negatively charged AgNPs may travel through the biofilm water channels, thereby affecting the whole biofilm structure. In contrast, positively charged Ag+ is bound at the cell surfaces and EPS, thus blocking its further flux within the biofilm layers. On the whole, the phototrophic biofilm demonstrated significant capacities to accumulate silver within the surface layers. The main mechanism to avoid the toxic effects is metal complexation with exopolysaccharides and accumulation within cell walls, especially pronounced under Ag+ stress. The significant AgNPs and Ag+ uptake capacities of phototrophic biofilm make it a highly resistant ecosystem in silver-polluted river waters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Barnett BP, Arepally A, Karmarkar PV, Qian D, Gilson WD, Walczak P, Howland V, Lawler L, Lauzon C, Stuber M (2007) Magnetic resonance-guided, real-time targeted delivery and imaging of magnetocapsules immunoprotecting pancreatic islet cells. Nat Med 13:986–991

    Article  CAS  Google Scholar 

  • Barriada JL, Tappin AD, Evans EH, Achterberg EP (2007) Dissolved silver measurements in seawater. TrAC Trends Anal Chem 26:809–817

    Article  CAS  Google Scholar 

  • Battin TJ, Kaplan LA, Newbold JD, Cheng X, Hansen C (2003) Effects of current velocity on the nascent architecture of stream microbial biofilms. Appl Environ Microbiol 69:5443–5452

    Article  CAS  Google Scholar 

  • Borrok D, Fein JB (2004) Distribution of protons and Cd between bacterial surfaces and dissolved humic substances determined through chemical equilibrium modelling. Geochim Cosmochim Acta 68:3043–3052

    Article  CAS  Google Scholar 

  • Boston H, Hill W (1991) Photosynthesis-light relations of stream periphyton communities. Limnol Oceanogr 36:644–656

    Article  CAS  Google Scholar 

  • Capek I (2004) Preparation of metal nanoparticles in water-in-oil (w/o) microemulsions. Adv Colloid Interf 110:49–74

    Article  CAS  Google Scholar 

  • Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–6156

    Article  CAS  Google Scholar 

  • Carlson C, Hussain S, Schrand A, Braydich-Stolle L, Hess K, Jones R, Schlager J (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 112:13608–13619

    Article  CAS  Google Scholar 

  • Chen C, Wen D, Wang J (2014) Cellular surface characteristics of Saccharomyces cerevisiae before and after Ag(I) biosorption. Bioresour Technol 156:380–383

    Article  CAS  Google Scholar 

  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

    Article  CAS  Google Scholar 

  • Dimkpa CO, Calder A, Gajjar P, Merugu S, Huang W, Britt DW, McLean JE, Johnson WP, Anderson AJ (2011) Interaction of silver nanoparticles with an environmentally beneficial bacterium, Pseudomonas chlororaphis. J Hazard Mater 188:428–435

    Article  CAS  Google Scholar 

  • El Badawy AM, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM (2010) Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 45:283–287

    Article  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(19):7285–7290

    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

    Article  CAS  Google Scholar 

  • Fein JB, Martin AM, Wightman PG (2001) Metal adsorption onto bacterial surfaces: development of a predictive approach. Geochim Cosmochim Acta 65:4267–4273

    Article  CAS  Google Scholar 

  • Feng Q, Wu J, Chen G, Cui F, Kim T, Kim J (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52:662–668

    Article  CAS  Google Scholar 

  • Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636

    CAS  Google Scholar 

  • Flegal AR, Brown CL, Squire S, Ross JRM, Scelfo GM, Hibdon S (2007) Spatial and temporal variations in silver contamination and toxicity in San Francisco Bay. Environ Res 105:34–52

    Article  CAS  Google Scholar 

  • Frattini A, Pellegri N, Nicastro D, Sanctis OD (2005) Effect of amine groups in the synthesis of Ag nanoparticles using aminosilanes. Mater Chem Phys 94:148–152

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    CAS  Google Scholar 

  • González AG, Pokrovsky O (2014) Metal adsorption on mosses: toward a universal adsorption model. J Colloid Interface Sci 415:169–178

    Article  Google Scholar 

  • González AG, Shirokova LS, Pokrovsky OS, Emnova EE, Martinez RE, Santana-Casiano JM, González-Dávila M, Pokrovski GS (2010) Adsorption of copper on Pseudomonas aureofaciens: protective role of surface exopolysaccharides. J Colloid Interface Sci 350:305–314

    Article  Google Scholar 

  • González AG, Pokrovsky OS, Jimenez-Villacorta F, Shirokova LS, Santana Casiano JM, González- Davila M, Emnova E (2014) Iron adsorption onto soil and aquatic bacteria: XAS structural study. Chem Geol 372:32–45

    Article  Google Scholar 

  • González-Dávila M (1995) The role of phytoplankton cells on the control of heavy metal concentration in seawater. Mar Chem 48:215–236

    Article  Google Scholar 

  • Gou N, Onnis-Hayden A, Gu AZ (2010) Mechanistic toxicity assessment of nanomaterials by whole-cell-array stress genes expression analysis. Environ Sci Technol 44:5964–5970

    Article  CAS  Google Scholar 

  • Ha J, Gelabert A, Spormann AM, Brown GE Jr (2010) Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74:1–15

    Article  CAS  Google Scholar 

  • He W, Zhou Y-T, Wamer WG, Boudreau MD, Yin J-J (2012) Mechanisms of the pH dependent generation of hydroxyl radicals and oxygen induced by Ag nanoparticles. Biomaterials 33:7547–7555

    Article  CAS  Google Scholar 

  • Hillebrand H, Sommer U (2000) Diversity of benthic microalgae in response to colonization time and eutrophication. Aquat Bot 67:221–236

    Article  Google Scholar 

  • Hwang ET, Lee JH, Chae YJ, Kim YS, Kim BC, Sang BI, Gu MB (2008) Analysis of the toxic mode of action of silver nanoparticles using stress-specific bioluminescent bacteria. Small 4:746–750

    Article  CAS  Google Scholar 

  • Ivask A, Bondarenko O, Jepihhina N, Kahru A (2010) Profiling of the reactive oxygen species-related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Anal Bioanal Chem 398:701–716

    Article  CAS  Google Scholar 

  • Kachynski AV, Kuzmin AN, Nyk M, Roy I, Prasad PN (2008) Zinc oxide nanocrystals for nonresonant nonlinear optical microscopy in biology and medicine. J Phys Chem C 112:10721–10724

    Article  CAS  Google Scholar 

  • Kalishwaralal K, BarathManiKanth S, Pandian SRK, Deepak V, Gurunathan S (2010) Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloid Surf B 79:340–344

    Article  CAS  Google Scholar 

  • Kittler S, Greulich C, Diendorf J, Koller M, Epple M (2010) Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mater 22:4548–4554

    Article  CAS  Google Scholar 

  • Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175

    Article  CAS  Google Scholar 

  • Lok C-N, Ho C-M, Chen R, He Q-Y, Yu W-Y, Sun H, Tam PK-H, Chiu J-F, Che C-M (2006) Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 5:916–924

    Article  CAS  Google Scholar 

  • Martinez RE, Pokrovsky OS, Schott J, Oelkers EH (2008) Surface charge and zeta-potential of metabolically active and dead cyanobacteria. J Colloid Interface Sci 323:317–325

    Article  CAS  Google Scholar 

  • Maynard A, Michelson E (2006) The nanotechnology consumer products inventory. Woodrow Wilson International Center for Scholars, Washington, DC, 23

    Google Scholar 

  • Miao AJ, Luo Z, Chen CS, Chin WC, Santschi PH, Quigg A (2010) Intracellular uptake: a possible mechanism for silver engineered nanoparticle toxicity to a freshwater alga Ochromonas danica. PLoS ONE 5:e.15196

    Article  Google Scholar 

  • Mohanty S, Mishra S, Jena P, Jacob B, Sarkar B, Sonawane A (2012) An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles. Nano-Nanotechnol 8:916–924

    Article  CAS  Google Scholar 

  • Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–976

    Article  CAS  Google Scholar 

  • Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346

    Article  CAS  Google Scholar 

  • Murdock JN, Dodds WK (2007) Linking benthic algal biomass to stream substratum topography. J Phycol 43:449–460

    Article  Google Scholar 

  • Navarro E, Baun A, Behra R, Hartmann N, Filser J, Miao A-J, Quigg A, Santschi P, Sigg L (2008a) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17(5):372–386

    Article  CAS  Google Scholar 

  • Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008b) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964

    Article  CAS  Google Scholar 

  • Niemeyer CM (2001) Nanoparticles, proteins, and nucleic acids: biotechnology meets materials science. Angew Chem Int Ed 40:4128–4158

    Article  CAS  Google Scholar 

  • Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45:1177–1183

    Article  CAS  Google Scholar 

  • Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823

    Article  Google Scholar 

  • Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Paule A, Lyautey E, Garabetian F, Rols J-L (2009) Autogenic versus environmental control during development of river biofilm. J Limnol 45:1–10

    Article  Google Scholar 

  • Paule A, Lauga B, Ten-Hage L, Morchain J, Duran R, Paul E, Rols J-L (2011) A photosynthetic rotating annular bioreactor (Taylor–Couette type flow) for phototrophic biofilm cultures. Water Res 45:6107–6118

    Article  CAS  Google Scholar 

  • Pavasupree S, Ngamsinlapasathian S, Nakajima M, Suzuki Y, Yoshikawa S (2006) Synthesis, characterization, photocatalytic activity and dye-sensitized solar cell performance of nanorods/nanoparticles TiO2 with mesoporous structure. J Photochem Photobiol A 184:163–169

    Article  CAS  Google Scholar 

  • Perelaer J, Hendriks CE, de Laat AW, Schubert US (2009) One-step inkjet printing of conductive silver tracks on polymer substrates. Nanotechnology 20:165303

    Article  Google Scholar 

  • Pokrovsky OS, Martinez RE, Golubev SV, Kompantseva EI, Shirokova LS (2008) Adsorption of metals and protons on Gloeocapsa sp. cyanobacteria: a surface speciation approach. Appl Geochem 23:2574–2588

    Article  CAS  Google Scholar 

  • Pokrovsky OS, Feurtet-Mazel A, Martinez RE, Morin S, Baudrimont M, Duong T, Coste M (2010) Experimental study of cadmium interaction with periphytic biofilms. Appl Geochem 25:418–427

    Article  CAS  Google Scholar 

  • Radzig MA, Nadtochenko VA, Koksharova OA, Kiwi J, Lipasova VA, Khmel IA (2013) Antibacterial effects of silver nanoparticles on Gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloid Surf B 102:300–306

    Article  CAS  Google Scholar 

  • Ranjard L, Poly F, Lata J-C, Mougel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    Article  CAS  Google Scholar 

  • Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ Toxicol Chem 18:89–108

    Article  CAS  Google Scholar 

  • Richaume A, Pourcelot A, Rama R, Nazaret S (2006) Évaluation des modifications quantitatives, qualitatives et fonctionnelles induites par la conservation de consortiums bactériens extraits de sols. Les actes du BRG 371–389

  • Rico M, López A, Santana-Casiano JM, González AG, González-Dávila M (2013) Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress. Limnol Oceanogr 58:144–152

    Article  CAS  Google Scholar 

  • Sañudo-Wilhelmy SA, Flegal AR (1992) Anthropogenic silver in the Southern California Bight: a new tracer of sewage in coastal waters. Environ Sci Tech 26:2147–2151

    Article  Google Scholar 

  • Schultz A, Boyle D, Chamot D, Ong K, Wilkinson K, McGeer J, Sunahara G, Goss G (2014) Aquatic toxicity of manufactured nanomaterials: challenges and recommendations for future toxicity testing. Environ Chem 11:207–226

    Article  CAS  Google Scholar 

  • SCOR-Unesco (1996) Determination of photosynthetic pigments in seawater. Monographs on Oceanographic Methodology, vol 1. Unesco, Paris, pp 11–18

  • 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

    Article  CAS  Google Scholar 

  • Tungittiplakorn W, Lion LW, Cohen C, Kim J-Y (2004) Engineered polymeric nanoparticles for soil remediation. Environ Sci Technol 38:1605–1610

    Article  CAS  Google Scholar 

  • Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton methodik. Mitt Int Ver Theor Angew Limnol 9:1–38

    Google Scholar 

  • van Hullebusch ED, Zandvoort MH, Lens PNL (2003) Metal immobilisation by biofilms: mechanisms and analytical tools. Rev Environ Sci Biotechnol 2:9–33

    Article  Google Scholar 

  • Wigginton NS, Titta A, Piccapietra F, Dobias J, Nesatyy VJ, Suter MJF, Bernier-Latmani R (2010) Binding of silver nanoparticles to bacterial proteins depends on surface modifications and inhibits enzymatic activity. Environ Sci Technol 44:2163–2168

    Article  CAS  Google Scholar 

  • Zhang Y, Chen Y, Westerhoff P, Crittenden J (2009) Impact of natural organic matter and divalent cations on the stability of aqueous nanoparticles. Water Res 43:4249–4257

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research work has been supported by Midi-Pyrénées Regional Council (France) within the program Gagilau (NoDAER-R93 90173), funding the postdoctoral fellowship for Aridane G. González. Support from BIO-GEO-CLIM grant of Russian Ministry of Science and Education (No. 14.B25.31.0001) and ANR CITTOXIC Nano are equally acknowledged.

Author information

Authors and Affiliations

  1. Université de Toulouse; UPS, INP; EcoLab (Laboratoire Écologie Fonctionnelle et Environnement), 118 route de Narbonne, 31062, Toulouse, France

    Aridane G. González, Stéphane Mombo, Joséphine Leflaive, Alexandre Lamy & Jean-Luc Rols

  2. EcoLab; CNRS, 31062, Toulouse, France

    Aridane G. González, Stéphane Mombo, Joséphine Leflaive, Alexandre Lamy & Jean-Luc Rols

  3. Université de Toulouse; UPS; GET (Géosciences Environnement Toulouse) UMR 5563 CNRS, 14 Avenue Edouard Belin, 31400, Toulouse, France

    Aridane G. González & Oleg S. Pokrovsky

  4. BIO-GEO-CLIM Laboratory, Tomsk State University, Tomsk, Russia

    Oleg S. Pokrovsky

Authors
  1. Aridane G. González
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stéphane Mombo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joséphine Leflaive
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandre Lamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oleg S. Pokrovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean-Luc Rols
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aridane G. González.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 358 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González, A.G., Mombo, S., Leflaive, J. et al. Silver nanoparticles impact phototrophic biofilm communities to a considerably higher degree than ionic silver. Environ Sci Pollut Res 22, 8412–8424 (2015). https://doi.org/10.1007/s11356-014-3978-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3978-1

Keywords

Search

Navigation