Surface-functionalization effects on uptake of fluorescent polystyrene nanoparticles by model biofilms

Abstract

A study was conducted to investigate the role of nanoparticle (NP) surface functionalization/charge on their uptake by biofilms. Biofilms, bacterial colonies attached to surfaces via extracellular polymers, are effective at removing suspended nanomaterials from the aqueous phase. However, the mechanisms regulating particle uptake are unknown. Here, it was shown that the mechanism was strongly dependent on the nanoparticle surface ionization, and not the core composition of the NP. Uptake experiments were conducted using laboratory-cultured biofilms. The biofilms were incubated in the presence of fluorescent polystyrene NPs with either negatively-charged surfaces (i.e. functionalized with sulfated (SO4 -NP) or carboxylated (COO-NP) groups) or positively-charged surfaces (functionalized with primary amines, Amine-P). Particles with negatively-charged sulfated surfaces associated most strongly to biofilms across all experimental conditions. Associations of positively-charged amine particles with biofilms were greatest at high ionic conditions resembling those of seawater, but were sensitive to changes in ionic strength. Sorption of COO-NPs was lowest, relative to other particle types, and was not sensitive to ionic strength. The results of this study support an emerging precedent that biofilms may be an effective player in the binding and sequestration of nanoparticles in aqueous systems.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Battin TJ, Kammer FVD, Weilhartner A, Ottofuelling S, Hofmann T (2009) Nanostructured TiO2: transport behavior and effects on aquatic microbial communities under environmental conditions. Environ Sci Technol 43:8098–8104

    Article  CAS  Google Scholar 

  2. Beveridge TJ (1989) Role of cellular design in bacterial metal accumulation and mineralization. Annu Rev Microbiol 43:147–171

    Article  CAS  Google Scholar 

  3. Bloem J, Veninga M, Shepherd J (1995) Fully automatic determination of soil bacterial numbers, cell volumes, and frequency of dividing cells by confocal laser scanning microscopy and image analysis. Appl Environ Microbiol 61:926–936

    CAS  Google Scholar 

  4. Böckelmann U, Manz W, Neu TR, Szewzyk U (2002) Investigation of lotic microbial aggregates by a combined technique of fluorescent in situ hybridization and lectin-binding-analysis. J Microbiol Meth 49:75–87

    Article  Google Scholar 

  5. Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT (2007) Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5:401–411

    Article  CAS  Google Scholar 

  6. Briandet R, Lacroix-Gueu P, Renault M, Lecart S, Meylheuc T, Bidnenko E, Steenkeste K, Bellon-Fontaine MN, Fontaine-Aupart MP (2008) Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl Environ Microb 74:2135–2143

    Article  CAS  Google Scholar 

  7. Decho AW (1990) Microbial exopolymer secretions in ocean environments—their role(s) in food webs and marine processes. Oceanogr Mar Biol Ann Rev 28:73–153

    Google Scholar 

  8. Decho AW, Kawaguchi T, Allison MA, Louchard EM, Reid RP, Stephens FC, Voss KJ, Wheatcroft RA, Taylor BB (2003) Sediment properties influencing upwelling spectral reflectance signatures: the “biofilm gel effect”. Limnol Oceanogr 48:431–443

    Article  Google Scholar 

  9. Donlan RM, Piede JA, Heyes CD, Sanii L, Murga R, Edmonds P, El-Sayed I, El-Sayed MA (2004) Model system for growing and quantifying Streptococcus pneumoniae biofilms in situ and in real time. Appl Environ Microb 70:4980–4988

    Article  CAS  Google Scholar 

  10. Fabrega J, Renshaw JC, Lead JR (2009) Interactions of silver nanoparticles with Pseudomonas putida biofilms. Environ Sci Technol 43:9004–9009

    Article  CAS  Google Scholar 

  11. Farre M, Gajda-Schrantz K, Kantiani L, Barcelo D (2009) Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 398:81–95

    Article  Google Scholar 

  12. Ferris FG, Schultze S, Witten TC, Fyfe WS, Beveridge TJ (1989) Metal interactions with microbial biofilms in acidic and neutral pH environments. Appl Environ Microb 55:1249–1257

    CAS  Google Scholar 

  13. Ferry JL, Craig P, Hexel C, Sisco P, Frey R, Pennington PL, Fulton MH, Scott IG, Decho AW, Kashiwada S, Murphy CJ, Shaw TJ (2009) Transfer of gold nanoparticles from the water column to the estuarine food web. Nat Nanotechnol 4:441–444

    Article  CAS  Google Scholar 

  14. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  Google Scholar 

  15. Foster LJR, Moy YP, Rogers PL (2000) Metal binding capabilities of Rhizobium etli and its extracellular polymeric substances. Biotechnol Lett 22:1757–1760

    Article  CAS  Google Scholar 

  16. Hetrick EM, Shin JH, Paul HS, Schoenfisch MH (2009) Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials 30:2782–2789

    Article  CAS  Google Scholar 

  17. Jang LK, Brand W, Resong M, Mainieri W, Geesey GG (1990) Feasibility of using alginate to absorb dissolved copper from aqueous-media. Environ Prog 9:269–274

    Article  CAS  Google Scholar 

  18. Kolodny LA, Willard DM, Carillo LL, Nelson MW, Van Orden A (2001) Spatially correlated fluorescence/AFM of individual nanosized particles and biomolecules. Anal Chem 73:1959–1966

    Article  CAS  Google Scholar 

  19. Lai SK, O’Hanlon DE, Harold S, Man ST, Wang YY, Cone R, Hanes J (2007) Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc Natl Acad Sci USA 104:1482–1487

    Article  CAS  Google Scholar 

  20. Lellouche J, Kahana E, Elias S, Gedanken A, Banin E (2009) Antibiofilm activity of nanosized magnesium fluoride. Biomaterials 30:5969–5978

    Article  CAS  Google Scholar 

  21. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci USA 105:14265–14270

    Article  CAS  Google Scholar 

  22. Mayer C, Moritz R, Kirschner C, Borchard W, Maibaum R, Wingender J, Flemming HC (1999) The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int J Biol Macromol 26:3–16

    Article  CAS  Google Scholar 

  23. Neal AL (2008) What can be inferred from bacterium-nanoparticle interactions about the potential consequences of environmental exposure to NPs? Ecotoxicology 17:362–371

    Article  CAS  Google Scholar 

  24. Spagnoli C, Korniakov A, Ulman A, Balazs EA, Lyubchenko YL, Cowman MK (2005) Hyaluronan conformations on surfaces: effect of surface charge and hydrophobicity. Carbohydr Res 340:929–941

    Article  CAS  Google Scholar 

  25. Stoodley P, Debeer D, Lewandowski Z (1994) Liquid flow in biofilm systems. Appl Environ Microb 60:2711–2716

    CAS  Google Scholar 

  26. Tong MP, Ding JL, Shen Y, Zhu PT (2010) Influence of biofilm on the transport of fullerene (C-60) NPs in porous media. Water Res 44:1094–1103

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Cathy Murphy (University of Illinois at Urbana-Champaign) for assistance in zeta-potential measurements. This work was supported by the University of South Carolina NanoCenter, and the National Science Foundation (BME-1032579). The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alan W. Decho.

Electronic supplementary material

Supplementary Material: Additional information is available on materials and methods, together with figures, tables, and references. This material is available through www.Springer.com.

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 195 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nevius, B.A., Chen, Y.P., Ferry, J.L. et al. Surface-functionalization effects on uptake of fluorescent polystyrene nanoparticles by model biofilms. Ecotoxicology 21, 2205–2213 (2012). https://doi.org/10.1007/s10646-012-0975-3

Download citation

Keywords

  • Functionalized-NPs
  • Bacteria
  • Biofilms
  • Sorption
  • EPS