The role of charge on the diffusion of solutes and nanoparticles (silicon nanocrystals, nTiO2, nAu) in a biofilm
Mahmood Golmohamadi A , Rhett J. Clark B , Jonathan G. C. Veinot B and Kevin J. Wilkinson A C
+ Author Affiliations
- Author Affiliations
A Department of Chemistry, University of Montreal, PO Box 6128, Succursale Centre-ville, Montréal, QC, H3C 3J7, Canada.
B Department of Chemistry, University of Alberta, 11227 Saskatchewan Drive, Edmonton, AB, T6G 2G2, Canada.
C Corresponding author. Email: kj.wilkinson@umontreal.ca
Environmental Chemistry 10(1) 34-41 https://doi.org/10.1071/EN12106
Submitted: 26 October 2012 Accepted: 10 December 2012 Published: 27 February 2013
Environmental context. The mobility and bioavailability of both contaminants and nutrients in the environment depends, to a large extent, on their diffusion. Because the majority of microorganisms in the environment are embedded in biofilms, it is essential to quantify diffusion in biofilms in order to evaluate the risk of emerging contaminants, including nanomaterials and charged solutes. This study quantifies diffusion, in a model environmental biofilm, for a number of model contaminants of variable size and charge.
Abstract. The effect of solute and biofilm charge on self-diffusion (Brownian motion) in biofilms is examined. Diffusion coefficients (D) of several model (fluorescent) solutes (rhodamine B; tetramethylrhodamine, methyl ester; Oregon Green 488 carboxylic acid, succinimidyl ester and Oregon Green 488 carboxylic acid) and nanoparticles (functionalised silicon, gold and titanium) were determined using fluorescence correlation spectroscopy (FCS). Somewhat surprisingly, little effect due to charge was observed on the diffusion measurements in the biofilms. Furthermore, the ratio of the diffusion coefficient in the biofilm with respect to that in water (Db/Dw) remained virtually constant across a wide range of ionic strengths (0.1–100 mM) for both negatively and positively charged probes. In contrast, the self-diffusion coefficients of nanoparticles with sizes >10 nm greatly decreased in the biofilms with respect to those in water. Furthermore, much larger nanoparticles (>66 nm) appeared to be completely excluded from the biofilms. The results indicated that for many oligotrophic biofilms in the environment, the diffusion of solutes and nanoparticles will be primarily controlled by obstruction rather than electrostatic interactions. The results also imply that most nanomaterials will become significantly less mobile and less bioavailable (to non-planktonic organisms) as they increase in size beyond ~10 nm.
Additional keywords: bacteria, contaminant mobility, fluorescence correlation spectroscopy, Pseudomonas fluorescens.
References
[1] S. S. Branda, A. Vik, L. Friedman, R. Kolter, Biofilms: the matrix revisited. Trends Microbiol. 2005, 13, 20.| Biofilms: the matrix revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvF2ntg%3D%3D&md5=88112b4ce1a6718295f35b376e3687b2CAS |
[2] J. W. Costerton, Z. Lewandowski, D. de Beer, D. Caldwell, D. Korber, G. James, Biofilms, the customized microniche. J. Bacteriol. 1994, 176, 2137.
| 1:STN:280:DyaK2c3gvFajuw%3D%3D&md5=0d50cbdb45f05b4dc00284d85c4a79dfCAS |
[3] H. C. Flemming, T. R. Neu, D. J. Wozniak, The EPS matrix: the ‘house of biofilm cells’. J. Bacteriol. 2007, 189, 7945.
| The EPS matrix: the ‘house of biofilm cells’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyht7zN&md5=4abba0db6701bb59061a10b75ef38b2bCAS |
[4] I. Sutherland, Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 2001, 147, 3.
| 1:CAS:528:DC%2BD3MXhtlWntbk%3D&md5=7fe4a07b99f1f59d553002b297947983CAS |
[5] P. S. Stewart, J. W. Costerton, Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358, 135.
| Antibiotic resistance of bacteria in biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1Shsbs%3D&md5=5bbb51425af98a1742ce799e81ee32faCAS |
[6] P. S. Stewart, Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 2002, 292, 107.
| Mechanisms of antibiotic resistance in bacterial biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVCqur4%3D&md5=bbff7227d2e34d162f1c79565373adfcCAS |
[7] J. W. Costerton, P. S. Stewart, E. P. Greenberg, Bacterial biofilms: a common cause of persistent infections. Science 1999, 284, 1318.
| Bacterial biofilms: a common cause of persistent infections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1Squ78%3D&md5=b3fadce67691685f469a31b6c0265d9cCAS |
[8] J. Buffle, K. J. Wilkinson, H. P. Van Leeuwen, Chemodynamics and bioavailability in natural waters. Environ. Sci. Technol. 2009, 43, 7170.
| Chemodynamics and bioavailability in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGgu7vE&md5=069df5737d9ba7e8f2eb6d9a7fef8148CAS |
[9] P. S. Stewart, A review of experimental measurements of effective diffusive permeabilities and effective diffusion coefficients in biofilms. Biotechnol. Bioeng. 1998, 59, 261.
| A review of experimental measurements of effective diffusive permeabilities and effective diffusion coefficients in biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFWhsbo%3D&md5=bc53350656eb2fc23e79ee6eab664abcCAS |
[10] T. A. Davis, E. J. Kalis, J. P. Pinheiro, R. M. Town, H. P. van Leeuwen, CdII speciation in alginate gels. Environ. Sci. Technol. 2008, 42, 7242.
| CdII speciation in alginate gels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOmt7zL&md5=f29f34c2d7a0e77c7ad1f278fa6fe5c1CAS |
[11] M. Golmohamadi, T. A. Davis, K. J. Wilkinson, Diffusion and partitioning of cations in an agarose hydrogel. J. Phys. Chem. A 2012, 116, 6505.
| Diffusion and partitioning of cations in an agarose hydrogel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt12ltbY%3D&md5=0002417de3cdc51eed8badd5a0ac4623CAS |
[12] T. J. Battin, F. V. D. Kammer, A. Weilhartner, S. Ottofuelling, T. Hofmann, Nanostructured TiO2: transport behavior and effects on aquatic microbial communities under environmental conditions. Environ. Sci. Technol. 2009, 43, 8098.
| Nanostructured TiO2: transport behavior and effects on aquatic microbial communities under environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1artbbL&md5=463e573b1963e2968bc433192a62dcdeCAS |
[13] J. L. Ferry, P. Craig, C. Hexel, P. Sisco, R. Frey, P. L. Pennington, M. H. Fulton, I. G. Scott, A. W. Decho, S. Kashiwada, C. J. Murphy, T. J. Shaw, Transfer of gold nanoparticles from the water column to the estuarine food web. Nat. Nanotechnol. 2009, 4, 441.
| Transfer of gold nanoparticles from the water column to the estuarine food web.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotFWht74%3D&md5=7d84d6ca21fa0a2aaa4a28a353aa9e18CAS |
[14] J. D. Bryers, F. Drummond, Local macromolecule diffusion coefficients in structurally non-uniform bacterial biofilms using fluorescence recovery after photobleaching (FRAP). Biotechnol. Bioeng. 1998, 60, 462.
| Local macromolecule diffusion coefficients in structurally non-uniform bacterial biofilms using fluorescence recovery after photobleaching (FRAP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvVyis7o%3D&md5=bfc55ab685541ded7c2ad93445451dcbCAS |
[15] T. T. Duong, S. Morin, M. Coste, O. Herlory, A. Feurtet-Mazel, A. Boudou, Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. Sci. Total Environ. 2010, 408, 552.
| Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVyqs7rP&md5=8616f36ea54abe7bdd374c5d47bce673CAS |
[16] L. Johansson, U. Skantze, J. E. Lofroth, Diffusion and interaction in gels and solutions. 2. Experimental results on the obstruction effect. Macromolecules 1991, 24, 6019.
| Diffusion and interaction in gels and solutions. 2. Experimental results on the obstruction effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmtV2isrw%3D&md5=b2b067fe39c779144af1845e1d7b9924CAS |
[17] C. Sandt, J. Barbeau, M.-A. Gagnon, M. Lafleur, Role of the ammonium group in the diffusion of quaternary ammonium compounds in Streptococcus mutans biofilms. J. Antimicrob. Chemother. 2007, 60, 1281.
| Role of the ammonium group in the diffusion of quaternary ammonium compounds in Streptococcus mutans biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKmtL%2FN&md5=bd2aa1b96a6b284390d7932014ef209fCAS |
[18] Z. Zhang, E. Nadezhina, K. J. Wilkinson, Quantifying diffusion in a biofilm of Streptococcus mutans. Antimicrob. Agents Chemother. 2011, 55, 1075.
| Quantifying diffusion in a biofilm of Streptococcus mutans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktlamtL4%3D&md5=3eb96dfb03f03aa85b506dd2a29a3069CAS |
[19] B. Amsden, Solute diffusion in hydrogels. An examination of the retardation effect. Polym. Gels Network 1998, 6, 13.
| Solute diffusion in hydrogels. An examination of the retardation effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVWlu7k%3D&md5=288e7a75bf32a6b43483c402ca258ce0CAS |
[20] E. J. Kalis, T. A. Davis, R. M. Town, H. P. van Leeuwen, Impact of ionic strength on CdII partitioning between alginate gel and aqueous media. Environ. Sci. Technol. 2009, 43, 1091.
| Impact of ionic strength on CdII partitioning between alginate gel and aqueous media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1anuw%3D%3D&md5=a1cc49f944fb5fd4869e3cc369b2ca33CAS |
[21] H.-J. Kim, E. L. Michael Gias, M. N. Jones, The adsorption of cationic liposomes to Staphylococcus aureus biofilms. Colloids Surf. A: Physicochem. Eng. Asp. 1999, 149, 561.
| The adsorption of cationic liposomes to Staphylococcus aureus biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisVehtL0%3D&md5=f843cebfae988c4ceafa350421e795a6CAS |
[22] K. Ahmed, P. Gribbon, M. N. Jones, The application of confocal microscopy to the study of liposome adsorption onto bacterial biofilms. J. Liposome Res. 2002, 12, 285.
| The application of confocal microscopy to the study of liposome adsorption onto bacterial biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFWgtA%3D%3D&md5=675fb0a854a8cc08d601475fe96493f1CAS |
[23] C. A. Gordon, N. A. Hodges, C. Marriott, Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother. 1988, 22, 667.
| Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjs1Kksw%3D%3D&md5=1248e6d64cee97a1a322ea4fca39f6b4CAS |
[24] W. W. Nichols, S. M. Dorrington, M. P. E. Slack, H. L. Walmsley, Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother. 1988, 32, 518.
| Inhibition of tobramycin diffusion by binding to alginate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitVWmu7Y%3D&md5=bcbef50fa493211cdbe08ce003c8cb86CAS |
[25] C. Campanac, L. Pineau, A. Payard, G. Baziard-Mouysset, C. Roques, Interactions between biocide cationic agents and bacterial biofilms. Antimicrob. Agents Chemother. 2002, 46, 1469.
| Interactions between biocide cationic agents and bacterial biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFKkt7o%3D&md5=d4678742e8a356def326b3680ab7b0b2CAS |
[26] L. Marcotte, H. Therien-Aubin, C. Sandt, J. Barbeau, M. Lafleur, Solute size effects on the diffusion in biofilms of Streptococcus mutans. Biofouling 2004, 20, 189.
| Solute size effects on the diffusion in biofilms of Streptococcus mutans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKru7%2FF&md5=088e850a1f1be5bbfe51bdcc27a63243CAS |
[27] E. Guiot, P. Georges, A. Brun, M. P. Fontaine-Aupart, M. N. Bellon-Fontaine, R. Briandet, Heterogeneity of diffusion inside microbial biofilms determined by fluorescence correlation spectroscopy under two-photon excitation. Photochem. Photobiol. 2002, 75, 570.
| Heterogeneity of diffusion inside microbial biofilms determined by fluorescence correlation spectroscopy under two-photon excitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslWqu7w%3D&md5=a70a122ad2a0f4b4a86ec0c1a99a3d74CAS |
[28] T. O. Peulen, K. J. Wilkinson, Diffusion of nanoparticles in a biofilm. Environ. Sci. Technol. 2011, 45, 3367.
| Diffusion of nanoparticles in a biofilm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVehsrY%3D&md5=215eb060577e036efdaff5ce355c057eCAS |
[29] E. L. Elson, D. Magde, Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers 1974, 13, 1.
| Fluorescence correlation spectroscopy. I. Conceptual basis and theory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXnsVKguw%3D%3D&md5=6a4f0677a641d2d83d4bc9d7fcb9ac1eCAS |
[30] D. Magde, E. L. Elson, W. W. Webb, Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers 1974, 13, 29.
| Fluorescence correlation spectroscopy. II. An experimental realization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXnsVKnsg%3D%3D&md5=39b0e207a6a270dca43bbdae263c1ad6CAS |
[31] N. Fatin-Rouge, K. Starchev, J. Buffle, Size effects on diffusion processes within agarose gels. Biophys. J. 2004, 86, 2710.
| Size effects on diffusion processes within agarose gels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVyjtLs%3D&md5=8e81100af27cdd453d1713e5d8ad50b4CAS |
[32] P. O. Gendron, F. Avaltroni, K. J. Wilkinson, Diffusion coefficients of several rhodamine derivatives as determined by pulsed field gradient-nuclear magnetic resonance and fluorescence correlation spectroscopy. J. Fluoresc. 2008, 18, 1093.
| Diffusion coefficients of several rhodamine derivatives as determined by pulsed field gradient-nuclear magnetic resonance and fluorescence correlation spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWjt7rN&md5=28411ee95eabec7f1c0c0179d47940faCAS |
[33] R. J. Clark, M. K. M. Dang, J. G. C. Veinot, Exploration of organic acid chain length on water-soluble silicon quantum dot surfaces. Langmuir 2010, 26, 15657.
| Exploration of organic acid chain length on water-soluble silicon quantum dot surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSls7nO&md5=86af31c94f89b4a21d8244f3a7f1bb34CAS |
[34] X. J. Leng, K. Starchev, J. Buffle, Adsorption of fluorescent dyes on oxide nanoparticles studied by fluorescence correlation spectroscopy. Langmuir 2002, 18, 7602.
| Adsorption of fluorescent dyes on oxide nanoparticles studied by fluorescence correlation spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1WmsLw%3D&md5=a41bd1f9f9cdd823b840526f02478e2eCAS |
[35] K. Monkos, Determination of the translational diffusion coefficient for proteins from the Stokes–Einstein Equation and viscometric measurements, in Some Aspects of Medical Physics – in Vivo and in Vitro Studies (Eds Z. Drzazga, K. Ślosarek) 2010, Polish Journal of Environmental Studies, Monographs Vol. 1, 83–89 (Hard Publishing Company: Olsztyn, Poland).
[36] M. R. Sangi, M. J. Halstead, K. A. Hunter, Use of the diffusion gradient thin film method to measure trace metals in fresh waters at low ionic strength. Anal. Chim. Acta 2002, 456, 241.
| Use of the diffusion gradient thin film method to measure trace metals in fresh waters at low ionic strength.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFWgt70%3D&md5=1329959735111206e4c80b2cd27e8f00CAS |
[37] G. A. O’Toole, To build a biofilm. J. Bacteriol. 2003, 185, 2687.
| To build a biofilm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Gnu7s%3D&md5=358591613f34eebec261f16040a18d45CAS |
[38] J. R. Lawrence, G. M. Wolfaardt, D. R. Korber, Determination of diffusion-coefficients in biofilms by confocal laser microscopy. Appl. Environ. Microbiol. 1994, 60, 1166.
| 1:STN:280:DC%2BC3crot1Khug%3D%3D&md5=ceab62744367d38fe3f30c68bd342126CAS |
[39] P. A. Suci, J. D. Vrany, M. W. Mittelman, Investigation of interactions between antimicrobial agents and bacterial biofilms using attenuated total reflection Fourier transform infrared spectroscopy. Biomaterials 1998, 19, 327.
| Investigation of interactions between antimicrobial agents and bacterial biofilms using attenuated total reflection Fourier transform infrared spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtlKqsbw%3D&md5=9cea67722d3fc01ee83a05627e96470bCAS |
[40] P. Lacroix-Gueu, R. Briandet, S. Leveque-Fort, M. N. Bellon-Fontaine, M. P. Fontaine-Aupart, In situ measurements of viral particles diffusion inside mucoid biofilms. C. R. Biol. 2005, 328, 1065.
| In situ measurements of viral particles diffusion inside mucoid biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OltrjM&md5=9bd63b13303b973a877198f56c395f2aCAS |
[41] T. Thurnheer, R. Gmur, S. Shapiro, B. Guggenheim, Mass transport of macromolecules within an in vitro model of supragingival plaque. Appl. Environ. Microbiol. 2003, 69, 1702.
| Mass transport of macromolecules within an in vitro model of supragingival plaque.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlClsbY%3D&md5=ed03514def7e2d66592b9f42816d972dCAS |
[42] O. Habimana, K. Steenkeste, M. P. Fontaine-Aupart, M. N. Bellon-Fontaine, S. Kulakauskas, R. Briandet, Diffusion of Nanoparticles in biofilms is altered by bacterial cell wall hydrophobicity. Appl. Environ. Microbiol. 2011, 77, 367.
| Diffusion of Nanoparticles in biofilms is altered by bacterial cell wall hydrophobicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVyjsro%3D&md5=4b0e8e94822ca29cd6895eadd226cb0fCAS |
[43] S. Takenaka, B. Pitts, H. M. Trivedi, P. S. Stewart, Diffusion of macromolecules in model oral biofilms. Appl. Environ. Microbiol. 2009, 75, 1750.
| Diffusion of macromolecules in model oral biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFKgtrs%3D&md5=89cc629bc2a18371b9d96e9a374cc7c7CAS |
[44] B. Dubertret, M. Calame, A. J. Libchaber, Single-mismatch detection using gold-quenched fluorescent oligonucleotides. Nat. Biotechnol. 2001, 19, 365.
| Single-mismatch detection using gold-quenched fluorescent oligonucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1Smsbk%3D&md5=f92d196bbaf8b520f39d8fcdb7e4e579CAS |
[45] J. J. Birmingham, N. P. Hughes, R. Treloar, Diffusion and binding measurements within oral biofilms using fluorescence photobleaching recovery methods. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1995, 350, 325.
| Diffusion and binding measurements within oral biofilms using fluorescence photobleaching recovery methods.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287psFelsg%3D%3D&md5=51f130b9d014e33e40f16f679744f2fdCAS |
[46] D. de Beer, P. Stoodley, Z. Lewandowski, Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 1997, 53, 151.
| Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVGktg%3D%3D&md5=3f9a86ece6f293c96d13377841ae45d7CAS |
