Electrophoresis as a simple method to detect deleterious actions of engineered nanoparticles on living cells
Elise Vouriot A , Isabelle Bihannic
A D , Audrey Beaussart A D , Yves Waldvogel A , Angelina Razafitianamaharavo A , Tania Ribeiro B , José Paulo S. Farinha B , Christophe Beloin C and Jérôme F. L. Duval A E
+ Author Affiliations
- Author Affiliations
A Université de Lorraine, CNRS, Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), UMR 7360, Vandoeuvre-lès-Nancy F-54501, France.
B Centro de Química-Física Molecular and IN - Institute of Nanoscience and Nanotechnology, Instituto Superior Técnico, University of Lisbon, 1049-001, Lisboa, Portugal.
C Institut Pasteur, Unité Génétique des Biofilms, F-75724 Paris 15, France.
D These authors equally contributed to this work.
E Corresponding author. Email: jerome.duval@univ-lorraine.fr
Environmental Chemistry 17(1) 39-53 https://doi.org/10.1071/EN19190
Submitted: 26 June 2019 Accepted: 7 August 2019 Published: 19 September 2019
Environmental context. Attractive interactions and subsequent contacts between nanoparticles and microorganisms are the first steps of a chain of events leading to adverse effects toward cells. We show that the electrophoretic response of complex mixtures of engineered nanoparticles and bacteria reflects initial nanoparticle-mediated cell surface damage. The technique is a promising option for rapid detection of deleterious actions of nanoparticles on biological cells.
Abstract. The release of engineered nanoparticles (NPs) to the environment may have profound implications for the health of aquatic biota. In this study, we show that the initial stage of the action of NPs on bacteria can be detected by the measurement of the electrophoretic fingerprints of mixed NP–cell dispersions. Such electrokinetic signatures reflect a modification of the physicochemical surface properties of both cells and NPs following changes in the organisation of the cell envelope, subsequent release of intracellular material and/or excretion of biomolecules. The demonstration is based on a thorough investigation of the electrohydrodynamic features of genetically engineered Escherichia coli bacteria with distinct surface phenotypes (presence of adhesive YeeJ large proteins or F-pili proteinaceous filaments) exposed to silica NPs (radius of 65 nm) functionalised by -NH2 terminal groups. At pH 7, electrostatics prevents interactions between bacteria and SiNH2 NPs, regardless of the considered concentration of NPs (range of 0–10−2 g L−1). At pH 3, electrostatically-driven interactions allow intimate contacts between NPs and bacteria. In turn, significant modulation of the electrophoretic determinants of cells and NPs are generated owing to the alteration of the cell envelope and acquisition of bio-corona by NPs. Differentiated roles of the cell surface appendages in the mediation of NP impacts are evidenced by the measured dependence of the electropherograms on cell surface phenotype and NP concentration. Cell morphology and surface roughness, evaluated by atomic force microscopy (AFM) in liquid, confirm the conditions of pH and concentration of NPs where NP–cell interactions are operational. The combination of electrokinetics and AFM further pinpoints heterogeneities in the cell response at the single cell and population scales. Altogether, the results show that electrophoresis is suitable to detect the preliminary stage of events leading to the toxicity of NPs towards microorganisms.
References
Beaussart A, Beloin C, Ghigo J-M, Chapot-Chartier M-P, Kulakauskas S, Duval JFL (2018a). Probing the influence of cell surface polysaccharides on nanodendrimer binding to Gram-negative and Gram-positive bacteria using single-nanoparticle force spectroscopy. Nanoscale 10, 12743–12753.| Probing the influence of cell surface polysaccharides on nanodendrimer binding to Gram-negative and Gram-positive bacteria using single-nanoparticle force spectroscopyCrossref | GoogleScholarGoogle Scholar | 29946619PubMed |
Beaussart A, Caillet C, Bihannic I, Zimmermann R, Duval JFL (2018b). Remarkable reversal of electrostatic interaction forces on zwitterionic soft nanointerfaces in a monovalent aqueous electrolyte: An AFM study at the single nanoparticle level. Nanoscale 10, 3181–3190.
| Remarkable reversal of electrostatic interaction forces on zwitterionic soft nanointerfaces in a monovalent aqueous electrolyte: An AFM study at the single nanoparticle levelCrossref | GoogleScholarGoogle Scholar | 29372221PubMed |
Beddoes CM, Case CP, Briscoe WH (2015). Understanding nanoparticle cellular entry: A physicochemical perspective. Advances in Colloid and Interface Science 218, 48–68.
| Understanding nanoparticle cellular entry: A physicochemical perspectiveCrossref | GoogleScholarGoogle Scholar | 25708746PubMed |
Beloin C, Roux A, Ghigo J (2008). Escherichia coli biofilms. Current Topics in Microbiology and Immunology 322, 249–289.
| Escherichia coli biofilmsCrossref | GoogleScholarGoogle Scholar | 18453280PubMed |
Beveridge TJ, Graham LL (1991). Surface layers of bacteria. Microbiological Reviews 55, 684–705.
Bolshakova AV, Kiselyova OI, Yaminsky IV (2004). Microbial surfaces investigated using atomic force microscopy. Biotechnology Progress 20, 1615–1622.
| Microbial surfaces investigated using atomic force microscopyCrossref | GoogleScholarGoogle Scholar | 15575691PubMed |
Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fiévet F (2006). Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Letters 6, 866–870.
| Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal mediumCrossref | GoogleScholarGoogle Scholar | 16608300PubMed |
Chai H, Yao J, Sun J, Zhang C, Liu W, Zhu M, Ceccanti B (2015). The effect of metal oxide nanoparticles on functional bacteria and metabolic profiles in agricultural soil. Bulletin of Environmental Contamination and Toxicology 94, 490–495.
| The effect of metal oxide nanoparticles on functional bacteria and metabolic profiles in agricultural soilCrossref | GoogleScholarGoogle Scholar | 25636440PubMed |
Chaveroche MK, Ghigo JM, D’Enfert C (2000). A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Research 28,
| A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulansCrossref | GoogleScholarGoogle Scholar | 11071951PubMed |
Chen Q, Yang S, Li Z (1999). Surface roughness evaluation by using wavelets analysis. Precision Engineering 23, 209–212.
| Surface roughness evaluation by using wavelets analysisCrossref | GoogleScholarGoogle Scholar |
Choi O, Yu C-P, Esteban Fernández G, Hu Z (2010). Interactions of nanosilver with Escherichia coli cells in planktonic and biofilm cultures. Water Research 44, 6095–6103.
| Interactions of nanosilver with Escherichia coli cells in planktonic and biofilm culturesCrossref | GoogleScholarGoogle Scholar | 20659752PubMed |
Colvin VL (2004). The potential environmental impact of engineered nanomaterials. Nature Biotechnology 22, 760
| The potential environmental impact of engineered nanomaterialsCrossref | GoogleScholarGoogle Scholar |
Costa TRD, Ilangovan A, Ukleja M, Redzej A, Santini JM, Smith TK, Egelman EH, Waksman G (2016). Structure of the bacterial sex F pilus reveals an assembly of a stoichiometric protein-phospholipid complex. Cell 166, 1436–1444.
| Structure of the bacterial sex F pilus reveals an assembly of a stoichiometric protein-phospholipid complexCrossref | GoogleScholarGoogle Scholar | 27610568PubMed |
Crucho CIC, Baleizão C, Farinha JPS (2017). Functional group coverage and conversion quantification in nanostructured silica by 1 H NMR. Analytical Chemistry 89, 681–687.
| Functional group coverage and conversion quantification in nanostructured silica by 1 H NMRCrossref | GoogleScholarGoogle Scholar |
Dague E, Duval J, Jorand F, Thomas F, Gaboriaud F (2006). Probing surface structures of Shewanella spp. by microelectrophoresis. Biophysical Journal 90, 2612–2621.
| Probing surface structures of Shewanella spp. by microelectrophoresisCrossref | GoogleScholarGoogle Scholar | 16415062PubMed |
Delgado AV, González-Caballero F, Hunter RJ, Koopal LK, Lyklema J (2005). Measurement and interpretation of electrokinetic phenomena (IUPAC Technical Report). Pure and Applied Chemistry 77, 1753–1805.
| Measurement and interpretation of electrokinetic phenomena (IUPAC Technical Report)Crossref | GoogleScholarGoogle Scholar |
Diallo MS, Christie S, Swaminathan P, Balogh L, Shi X, Um W, Papelis C, Iii WAG, Johnson JH (2004). Dendritic chelating agents. 1. Cu(II) binding to ethylene diamine core poly(amidoamine) dendrimers in aqueous solutions. Langmuir 20, 2640–2651.
| Dendritic chelating agents. 1. Cu(II) binding to ethylene diamine core poly(amidoamine) dendrimers in aqueous solutionsCrossref | GoogleScholarGoogle Scholar | 15835132PubMed |
Dubey RC, Maheshwari DK (1999). ‘A textbook of microbiology.’ (S. Chand Publishing & Company Ltd: New Delhi, India)
Dufrêne YF (2008). Towards nanomicrobiology using atomic force microscopy. Nature Reviews. Microbiology 6, 674–680.
| Towards nanomicrobiology using atomic force microscopyCrossref | GoogleScholarGoogle Scholar | 18622407PubMed |
Duval JFL (2017). Chemodynamics of metal ion complexation by charged nanoparticles: A dimensionless rationale for soft, core-shell and hard particle types. Physical Chemistry Chemical Physics 19, 11802–11815.
| Chemodynamics of metal ion complexation by charged nanoparticles: A dimensionless rationale for soft, core-shell and hard particle typesCrossref | GoogleScholarGoogle Scholar | 28447689PubMed |
Duval JFL, Gaboriaud F (2010). Progress in electrohydrodynamics of soft microbial particle interphases. Current Opinion in Colloid & Interface Science 15, 184–195.
| Progress in electrohydrodynamics of soft microbial particle interphasesCrossref | GoogleScholarGoogle Scholar |
Duval JFL, Ohshima H (2006). Electrophoresis of diffuse soft particles. Langmuir 22, 3533–3546.
| Electrophoresis of diffuse soft particlesCrossref | GoogleScholarGoogle Scholar |
Duval JFL, Leermakers FAM, Van Leeuwen HP (2004). Electrostatic interactions between double layers: Influence of surface roughness, regulation, and chemical heterogeneities. Langmuir 20, 5052–5065.
| Electrostatic interactions between double layers: Influence of surface roughness, regulation, and chemical heterogeneitiesCrossref | GoogleScholarGoogle Scholar |
Duval JFL, Farinha JPS, Pinheiro JP (2013). Impact of electrostatics on the chemodynamics of highly charged metal–polymer nanoparticle complexes. Langmuir 29, 13821–13835.
| Impact of electrostatics on the chemodynamics of highly charged metal–polymer nanoparticle complexesCrossref | GoogleScholarGoogle Scholar |
El Badawy AM, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM (2011). Surface charge-dependent toxicity of silver nanoparticles. Environmental Science & Technology 45, 283–287.
| Surface charge-dependent toxicity of silver nanoparticlesCrossref | GoogleScholarGoogle Scholar |
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016). Biofilms: An emergent form of bacterial life. Nature Reviews. Microbiology 14, 563–575.
| Biofilms: An emergent form of bacterial lifeCrossref | GoogleScholarGoogle Scholar | 27510863PubMed |
Francius G, Polyakov P, Merlin J, Abe Y, Ghigo JM, Merlin C, Beloin C, Duval JFL (2011). Bacterial surface appendages strongly impact nanomechanical and electrokinetic properties of Escherichia coli cells subjected to osmotic stress. PLoS One 6, e20066
| Bacterial surface appendages strongly impact nanomechanical and electrokinetic properties of Escherichia coli cells subjected to osmotic stressCrossref | GoogleScholarGoogle Scholar | 21655293PubMed |
Geusebroek J, Smeulders AWM, van de Weijer J (2003). Fast anisotropic gauss filtering. IEEE Transactions on Image Processing 12, 938–943.
Hardij J, Cecchet F, Berquand A, Gheldof D, Chatelain C, Mullier F, Chatelain B, Hardij J, Cecchet F, Berquand A, Gheldof D, Chatelain C (2013). Characterisation of tissue factor-bearing extracellular vesicles with AFM: Comparison of air-tapping-mode AFM and liquid Peak Force AFM. Journal of Extracellular Vesicles 2, 21045
| Characterisation of tissue factor-bearing extracellular vesicles with AFM: Comparison of air-tapping-mode AFM and liquid Peak Force AFMCrossref | GoogleScholarGoogle Scholar |
Hartlen KD, Athanasopoulos APT, Kitaev V (2008). Facile preparation of highly monodisperse small silica spheres (15 to >200 nm) suitable for colloidal templating and formation of ordered arrays. Langmuir 24, 1714–1720.
| Facile preparation of highly monodisperse small silica spheres (15 to >200 nm) suitable for colloidal templating and formation of ordered arraysCrossref | GoogleScholarGoogle Scholar | 18225928PubMed |
Hayden SC, Zhao G, Saha K, Phillips RL, Li X, Miranda OR, Rotello VM, El-Sayed MA, Schmidt-Krey I, Bunz UHF (2012). Aggregation and interaction of cationic nanoparticles on bacterial surfaces. Journal of the American Chemical Society 134, 6920–6923.
| Aggregation and interaction of cationic nanoparticles on bacterial surfacesCrossref | GoogleScholarGoogle Scholar | 22489570PubMed |
Hill RJ, Saville DA, Russel WB (2003). Electrophoresis of spherical polymer-coated colloidal particles. Journal of Colloid and Interface Science 258, 56–74.
| Electrophoresis of spherical polymer-coated colloidal particlesCrossref | GoogleScholarGoogle Scholar |
Huang Z, Zheng X, Yan D, Yin G, Liao X, Kang Y, Yao Y, Huang D, Hao B (2008). Toxicological effect of ZnO nanoparticles based on bacteria. Langmuir 24, 4140–4144.
| Toxicological effect of ZnO nanoparticles based on bacteriaCrossref | GoogleScholarGoogle Scholar | 18341364PubMed |
Ikuma K, Decho AW, Lau BLT (2015). When nanoparticles meet biofilms-interactions guiding the environmental fate and accumulation of nanoparticles. Frontiers in Microbiology 6, 1–6.
| When nanoparticles meet biofilms-interactions guiding the environmental fate and accumulation of nanoparticlesCrossref | GoogleScholarGoogle Scholar |
Ingale AG, Chaudhari AN (2013). Biogenic synthesis of nanoparticles and potential applications : an eco-friendly approach. Journal of Nanomedicine and Nanotechnology 4,
| Biogenic synthesis of nanoparticles and potential applications : an eco-friendly approachCrossref | GoogleScholarGoogle Scholar |
Jacobson KH, Gunsolus IL, Kuech TR, Troiano JM, Melby ES, Lohse SE, Hu D, Chrisler WB, Murphy CJ, Orr G, Geiger FM, Haynes CL, Pedersen JA (2015). Lipopolysaccharide density and structure govern the extent and distance of nanoparticle interaction with actual and model bacterial outer membranes. Environmental Science & Technology 49, 10642–10650.
| Lipopolysaccharide density and structure govern the extent and distance of nanoparticle interaction with actual and model bacterial outer membranesCrossref | GoogleScholarGoogle Scholar |
Jandt KD (2001). Atomic force microscopy of biomaterials surfaces and interfaces. Surface Science 491, 303–332.
| Atomic force microscopy of biomaterials surfaces and interfacesCrossref | GoogleScholarGoogle Scholar |
Jiang W, Yang K, Vachet RW, Xing B (2010). Interaction between oxide nanoparticles and biomolecules of the bacterial cell envelope as examined by infrared spectroscopy. Langmuir 26, 18071–18077.
| Interaction between oxide nanoparticles and biomolecules of the bacterial cell envelope as examined by infrared spectroscopyCrossref | GoogleScholarGoogle Scholar | 21062006PubMed |
Ju-Nam Y, Lead JR (2008). Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implications. The Science of the Total Environment 400, 396–414.
| Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implicationsCrossref | GoogleScholarGoogle Scholar | 18715626PubMed |
Kimkes TEP, Heinemann M (2018). Reassessing the role of the Escherichia coli CpxAR system in sensing surface contact. PLoS One 13, e0207181
| Reassessing the role of the Escherichia coli CpxAR system in sensing surface contactCrossref | GoogleScholarGoogle Scholar | 30412611PubMed |
Kleinstreuer NC, Sullivan K, Allen D, Edwards S, Mendrick DL, Embry M, Matheson J, Rowlands JC, Munn S, Maull E, Casey W (2016). Adverse outcome pathways: From research to regulation scientific workshop report. Regulatory Toxicology and Pharmacology 76, 39–50.
| Adverse outcome pathways: From research to regulation scientific workshop reportCrossref | GoogleScholarGoogle Scholar | 26774756PubMed |
Li N, Zeng S, He L, Zhong W (2010). Probing nanoparticle-protein interaction by capillary electrophoresis. Analytical Chemistry 82, 7460–7466.
| Probing nanoparticle-protein interaction by capillary electrophoresisCrossref | GoogleScholarGoogle Scholar | 20672831PubMed |
López-León T, Carvalho ELS, Seijo B, Ortega-Vinuesa JL, Bastos-González D (2005). Physicochemical characterization of chitosan nanoparticles: Electrokinetic and stability behavior. Journal of Colloid and Interface Science 283, 344–351.
| Physicochemical characterization of chitosan nanoparticles: Electrokinetic and stability behaviorCrossref | GoogleScholarGoogle Scholar | 15721903PubMed |
López-Viota J, Mandal S, Delgado AV, Toca-Herrera JL, Möller M, Zanuttin F, Balestrino M, Krol S (2009). Electrophoretic characterization of gold nanoparticles functionalized with human serum albumin (HSA) and creatine. Journal of Colloid and Interface Science 332, 215–223.
| Electrophoretic characterization of gold nanoparticles functionalized with human serum albumin (HSA) and creatineCrossref | GoogleScholarGoogle Scholar | 19155019PubMed |
Majdalani N, Heck M, Stout V, Gottesman S (2005). Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. Journal of Bacteriology 187, 6770–6778.
| Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coliCrossref | GoogleScholarGoogle Scholar | 16166540PubMed |
Martinez-Gil M, Goh KGK, Rackaityte E, Sakamoto C, Audrain B, Moriel DG, Totsika M, Ghigo JM, Schembri MA, Beloin C (2017). YeeJ is an inverse autotransporter from Escherichia coli that binds to peptidoglycan and promotes biofilm formation. Scientific Reports 7, 11326
| YeeJ is an inverse autotransporter from Escherichia coli that binds to peptidoglycan and promotes biofilm formationCrossref | GoogleScholarGoogle Scholar | 28900103PubMed |
Mathelié-Guinlet M (2017). Etude de l’intéraction nanoparticules-bactéries: application à l’élaboration d’un biocapteur. PhD thesis, Université de Bordeaux.
Mathelié-Guinlet M, Béven L, Moroté F, Moynet D, Grauby-Heywang C, Gammoudi I, Delville MH, Cohen-Bouhacina T (2017). Probing the threshold of membrane damage and cytotoxicity effects induced by silica nanoparticles in Escherichia coli bacteria. Advances in Colloid and Interface Science 245, 81–91.
| Probing the threshold of membrane damage and cytotoxicity effects induced by silica nanoparticles in Escherichia coli bacteriaCrossref | GoogleScholarGoogle Scholar | 28477864PubMed |
Mathelié-Guinlet M, Grauby-Heywang C, Martin A, Février H, Moroté F, Vilquin A, Béven L, Delville MH, Cohen-Bouhacina T (2018). Detrimental impact of silica nanoparticles on the nanomechanical properties of Escherichia coli, studied by AFM. Journal of Colloid and Interface Science 529, 53–64.
| Detrimental impact of silica nanoparticles on the nanomechanical properties of Escherichia coli, studied by AFMCrossref | GoogleScholarGoogle Scholar | 29883930PubMed |
Maurya SK, Gopmandal PP, Ohshima H (2018). Electrophoresis of concentrated suspension of soft particles with volumetrically charged inner core. Colloid & Polymer Science 296, 721–732.
| Electrophoresis of concentrated suspension of soft particles with volumetrically charged inner coreCrossref | GoogleScholarGoogle Scholar |
McBroom AJ, Kuehn MJ (2007). Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Molecular Microbiology 63, 545–558.
| Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress responseCrossref | GoogleScholarGoogle Scholar | 17163978PubMed |
Mecke A, Majoros IJ, Patri AK, Baker JR, Banaszak Holl MM, Orr BG (2005). Lipid bilayer disruption by polycationic polymers: The roles of size and chemical functional group. Langmuir 21, 10348–10354.
| Lipid bilayer disruption by polycationic polymers: The roles of size and chemical functional groupCrossref | GoogleScholarGoogle Scholar | 16262291PubMed |
Monopoli MP, Åberg C, Salvati A, Dawson KA (2012). Biomolecular coronas provide the biological identity of nanosized materials. Nature Nanotechnology 7, 779–786.
| Biomolecular coronas provide the biological identity of nanosized materialsCrossref | GoogleScholarGoogle Scholar | 23212421PubMed |
Moore MN (2006). Do nanoparticles present ecotoxicological risks for the health of the aquatic environment?. Environment International 32, 967–976.
| Do nanoparticles present ecotoxicological risks for the health of the aquatic environment?Crossref | GoogleScholarGoogle Scholar | 16859745PubMed |
Moussa M, Caillet C, Town RM, Duval JFL (2015). Remarkable electrokinetic features of charge-stratified soft nanoparticles: Mobility reversal in monovalent aqueous electrolyte. Langmuir 31, 5656–5666.
| Remarkable electrokinetic features of charge-stratified soft nanoparticles: Mobility reversal in monovalent aqueous electrolyteCrossref | GoogleScholarGoogle Scholar | 25939023PubMed |
Neal AL (2008). What can be inferred from bacterium-nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles?. Ecotoxicology 17, 362–371.
| What can be inferred from bacterium-nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles?Crossref | GoogleScholarGoogle Scholar | 18454313PubMed |
Ohshima H (1995). Electrophoresis of soft particles. Advances in Colloid and Interface Science 62, 189–235.
| Electrophoresis of soft particlesCrossref | GoogleScholarGoogle Scholar |
Pagnout C, Jomini S, Dadhwal M, Caillet C, Thomas F, Bauda P (2012). Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward Escherichia coli. Colloids and Surfaces. B, Biointerfaces 92, 315–321.
| Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward Escherichia coliCrossref | GoogleScholarGoogle Scholar | 22218337PubMed |
Peulen TO, Wilkinson KJ (2011). Diffusion of nanoparticles in a biofilm. Environmental Science & Technology 45, 3367–3373.
| Diffusion of nanoparticles in a biofilmCrossref | GoogleScholarGoogle Scholar |
Phillips RL, Miranda OR, You CC, Rotello VM, Bunz UHF (2008). Rapid and efficient identification of bacteria using gold-nanoparticle-poly(para-phenyleneethynylene) constructs. Angewandte Chemie International Edition 47, 2590–2594.
| Rapid and efficient identification of bacteria using gold-nanoparticle-poly(para-phenyleneethynylene) constructsCrossref | GoogleScholarGoogle Scholar | 18228547PubMed |
Planchon M, Ferrari R, Guyot F, Gélabert A, Menguy N, Chanéac C, Thill A, Benedetti MF, Spalla O (2013). Interaction between Escherichia coli and TiO2 nanoparticles in natural and artificial waters. Colloids and Surfaces. B, Biointerfaces 102, 158–164.
| Interaction between Escherichia coli and TiO2 nanoparticles in natural and artificial watersCrossref | GoogleScholarGoogle Scholar | 23006561PubMed |
Reisner A, Haagensen JAJ, Schembri MA, Zechner EL, Molin S (2003). Development and maturation of Escherichia coli K-12 biofilms. Molecular Microbiology 48, 933–946.
| Development and maturation of Escherichia coli K-12 biofilmsCrossref | GoogleScholarGoogle Scholar | 12753187PubMed |
Ribeiro T, Raja S, Rodrigues AS, Fernandes F, Baleizão C, Farinha JPS (2014). NIR and visible perylenediimide-silica nanoparticles for laser scanning bioimaging. Dyes and Pigments 110, 227–234.
| NIR and visible perylenediimide-silica nanoparticles for laser scanning bioimagingCrossref | GoogleScholarGoogle Scholar |
Ribeiro T, Baleizão C, Farinha JPS (2017). Artefact-free evaluation of metal enhanced fluorescence in silica coated gold nanoparticles. Scientific Reports 7, 2440
| Artefact-free evaluation of metal enhanced fluorescence in silica coated gold nanoparticlesCrossref | GoogleScholarGoogle Scholar | 28550301PubMed |
Rowenczyk L, Duclairoir-poc C, Barreau M, Picard C, Hucher N, Orange N, Grisel M, Feuilloley M (2017). Impact of coated TiO2-nanoparticles used in sunscreens on two representative strains of the human microbiota : Effect of the particle surface nature and aging. Colloids and Surfaces. B, Biointerfaces 158, 339–348.
| Impact of coated TiO2-nanoparticles used in sunscreens on two representative strains of the human microbiota : Effect of the particle surface nature and agingCrossref | GoogleScholarGoogle Scholar | 28715765PubMed |
Shang L, Nienhaus K, Nienhaus GU (2014). Engineered nanoparticles interacting with cells: Size matters. Journal of Nanobiotechnology 12, 5
| Engineered nanoparticles interacting with cells: Size mattersCrossref | GoogleScholarGoogle Scholar | 24491160PubMed |
Sheng GP, Yu HQ, Yue ZB (2005). Production of extracellular polymeric substances from Rhodopseudomonas acidophila in the presence of toxic substances. Applied Microbiology and Biotechnology 69, 216–222.
| Production of extracellular polymeric substances from Rhodopseudomonas acidophila in the presence of toxic substancesCrossref | GoogleScholarGoogle Scholar | 15843928PubMed |
Shrivastava S, Bera T, Roy A (2007). Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18,
| Characterization of enhanced antibacterial effects of novel silver nanoparticlesCrossref | GoogleScholarGoogle Scholar |
Silva T, Pokhrel LR, Dubey B, Tolaymat TM, Maier KJ, Liu X (2014). Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: Comparison between general linear model-predicted and observed toxicity. The Science of the Total Environment 468–469, 968–976.
| Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: Comparison between general linear model-predicted and observed toxicityCrossref | GoogleScholarGoogle Scholar | 24091120PubMed |
Silverman PM (1997). Towards a structural biology of bacterial conjugation. Molecular Microbiology 23, 423–429.
| Towards a structural biology of bacterial conjugationCrossref | GoogleScholarGoogle Scholar | 9044277PubMed |
Škvarla J (2007). Hard versus soft particle electrokinetics of silica colloids. Langmuir 23, 5305–5314.
| Hard versus soft particle electrokinetics of silica colloidsCrossref | GoogleScholarGoogle Scholar | 17417889PubMed |
Stöber W, Fink A, Bohn E (1968). Controlled growth of monodisperse silica spheres in the micron size range. Journal of Colloid and Interface Science 26, 62–69.
| Controlled growth of monodisperse silica spheres in the micron size rangeCrossref | GoogleScholarGoogle Scholar |
Stoimenov PK, Klinger RL, Marchin GL, Klabunde KJ (2002). Metal oxide nanoparticles as bactericidal agents. Langmuir 18, 6679–6686.
| Metal oxide nanoparticles as bactericidal agentsCrossref | GoogleScholarGoogle Scholar |
Svenson S (2009). Dendrimers as versatile platform in drug delivery applications. European Journal of Pharmaceutics and Biopharmaceutics 71, 445–462.
| Dendrimers as versatile platform in drug delivery applicationsCrossref | GoogleScholarGoogle Scholar | 18976707PubMed |
Tajarobi F, El-Sayed M, Rege BD, Polli JE, Ghandehari H (2001). Transport of poly amidoamine dendrimers across Madin-Darby canine kidney cells. International Journal of Pharmaceutics 215, 263–267.
| Transport of poly amidoamine dendrimers across Madin-Darby canine kidney cellsCrossref | GoogleScholarGoogle Scholar | 11250111PubMed |
Thill A, Zeyons O, Spalla O, Chauvat F, Rose J, Auffan M, Flank AM (2006). Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanism. Environmental Science & Technology 40, 6151–6156.
| Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanismCrossref | GoogleScholarGoogle Scholar |
van der Wal A, Norde W, Zehnder AJB, Lyklema J (1997). Determination of the total charge in the cell walls of Gram-positive bacteria. Colloids and Surfaces. B, Biointerfaces 9, 81–100.
| Determination of the total charge in the cell walls of Gram-positive bacteriaCrossref | GoogleScholarGoogle Scholar |
van Loosdrecht MCM, Lyklema J, Norde W, Zehnder AJB (1990). Influence of interfaces on microbial activity. Microbiological Reviews 54, 75–87.
Velzeboer I, Hendriks AJ, Ragas MJ, De Meent D (2008). Nanomaterials in the environment aquatic ecotoxicity tests of some nanomaterials. Environmental Toxicology and Chemistry 27, 1942–1947.
| Nanomaterials in the environment aquatic ecotoxicity tests of some nanomaterialsCrossref | GoogleScholarGoogle Scholar | 19086210PubMed |
Wang YA, Yu X, Silverman PM, Harris RL, Egelman EH (2009). The structure of F-pili. Journal of Molecular Biology 385, 22–29.
| The structure of F-piliCrossref | GoogleScholarGoogle Scholar | 18992755PubMed |
Yang Y, Quensen J, Mathieu J, Wang Q, Wang J, Li M, Tiedje JM, Alvarez PJJ (2014). Pyrosequencing reveals higher impact of silver nanoparticles than Ag+ on the microbial community structure of activated sludge. Water Research 48, 317–325.
| Pyrosequencing reveals higher impact of silver nanoparticles than Ag+ on the microbial community structure of activated sludgeCrossref | GoogleScholarGoogle Scholar | 24120408PubMed |
Zeyons O, Thill A, Chauvat F, Menguy N, Cassier-Chauvat C, Oréar C, Daraspe J, Auffan M, Rose J, Spalla O (2009). Direct and indirect CeO2 nanoparticles toxicity for Escherichia coli and Synechocystis. Nanotoxicology 3, 284–295.
| Direct and indirect CeO2 nanoparticles toxicity for Escherichia coli and SynechocystisCrossref | GoogleScholarGoogle Scholar |
