Interaction of Graphene Oxide with Bacterial Cell Membranes: Insights from Force Spectroscopy

Understanding the interactions of graphene oxide (GO) with biological membranes is crucial for the evaluation of GO’s health and environmental impacts, its bactericidal activity, and to advance graphene-based biological and environmental applications. In an effort to understand graphene-induced bacterial inactivation, we studied the interaction of GO with bacterial (Escherichia coli) cell membranes using atomic force microscopy (AFM). Toward this goal, we devised a polydopamine-assisted experimental protocol to functionalize an AFM probe with GO nanosheets, and used AFM-based force spectroscopy to measure cell membrane–GO interaction forces. Our results show that GO–cell interactions are predominantly repulsive, with only sporadic adhesion forces being measured upon probe pull-off, which we attribute to lipopolysaccharide bridging. We provide evidence of the acellular oxidation of glutathione by GO, underscoring the role of oxidative pathways in GO-mediated bacterial cell inactivation. Our force spectrosc...

[1]  Menachem Elimelech,et al.  Antibacterial effects of carbon nanotubes: size does matter! , 2008, Langmuir : the ACS journal of surfaces and colloids.

[2]  A. Simchi,et al.  Flexible bactericidal graphene oxide–chitosan layers for stem cell proliferation , 2014 .

[3]  Yang Xu,et al.  Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. , 2010, ACS nano.

[4]  P. Sens,et al.  Two-chamber AFM: probing membrane proteins separating two aqueous compartments , 2006, Nature Methods.

[5]  A. D. Todd,et al.  Harnessing the chemistry of graphene oxide. , 2014, Chemical Society reviews.

[6]  Li Wei,et al.  Sharper and faster "nano darts" kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. , 2009, ACS nano.

[7]  I. V. Grigorieva,et al.  Precise and Ultrafast Molecular Sieving Through Graphene Oxide Membranes , 2014, Science.

[8]  Chunhai Fan,et al.  Graphene-based antibacterial paper. , 2010, ACS nano.

[9]  R. Ruoff,et al.  Poly(vinyl alcohol) reinforced and toughened with poly(dopamine)-treated graphene oxide, and its use for humidity sensing. , 2014, ACS nano.

[10]  J. Kysar,et al.  Measurement of the Elastic Properties and Intrinsic Strength of Monolayer Graphene , 2008, Science.

[11]  Haeshin Lee,et al.  Mussel-Inspired Surface Chemistry for Multifunctional Coatings , 2007, Science.

[12]  E. Ron,et al.  Changes in cell dimensions during amino acid starvation of Escherichia coli , 1982, Journal of bacteriology.

[13]  J. Gergely,et al.  Zero-length crosslinking procedure with the use of active esters. , 1990, Analytical biochemistry.

[14]  M. Elimelech,et al.  Relevance of electrokinetic theory for "soft" particles to bacterial cells: implications for bacterial adhesion. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[15]  Menachem Elimelech,et al.  Thin-Film Composite Polyamide Membranes Functionalized with Biocidal Graphene Oxide Nanosheets , 2014 .

[16]  Haitao Liu,et al.  Availability of the basal planes of graphene oxide determines whether it is antibacterial. , 2014, ACS applied materials & interfaces.

[17]  J. Tascón,et al.  Graphene oxide dispersions in organic solvents. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[18]  B. Logan,et al.  Probing Bacterial Electrosteric Interactions Using Atomic Force Microscopy , 2000 .

[19]  M. Mirjalili,et al.  Using graphene/TiO2 nanocomposite as a new route for preparation of electroconductive, self-cleaning, antibacterial and antifungal cotton fabric without toxicity , 2014, Cellulose.

[20]  K. Young,et al.  Penicillin Binding Protein 5 Affects Cell Diameter, Contour, and Morphology of Escherichia coli , 2000, Journal of bacteriology.

[21]  Heyou Han,et al.  A new function of graphene oxide emerges: inactivating phytopathogenic bacterium Xanthomonas oryzae pv. Oryzae , 2013, Journal of Nanoparticle Research.

[22]  H. Butt,et al.  Measuring surface forces in aqueous electrolyte solution with the atomic force microscope , 1995 .

[23]  Baoxia Mi,et al.  Layer-by-layer assembly of graphene oxide membranes via electrostatic interaction , 2014 .

[24]  G. Wallace,et al.  Processable aqueous dispersions of graphene nanosheets. , 2008, Nature nanotechnology.

[25]  Wei Gao,et al.  New insights into the structure and reduction of graphite oxide. , 2009, Nature chemistry.

[26]  Agnes B Kane,et al.  Biological interactions of graphene-family nanomaterials: an interdisciplinary review. , 2012, Chemical research in toxicology.

[27]  F. Besenbacher,et al.  Immobilisation of living bacteria for AFM imaging under physiological conditions. , 2010, Ultramicroscopy.

[28]  B. Freeman,et al.  Elucidating the structure of poly(dopamine). , 2012, Langmuir : the ACS journal of surfaces and colloids.

[29]  Jing Kong,et al.  Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. , 2011, ACS nano.

[30]  K. Novoselov,et al.  Exploring the Interface of Graphene and Biology , 2014, Science.

[31]  Feng Zhou,et al.  Highly selective uptake and release of charged molecules by pH-responsive polydopamine microcapsules. , 2011, Macromolecular bioscience.

[32]  Cher Ming Tan,et al.  Antibacterial action of dispersed single-walled carbon nanotubes on Escherichia coli and Bacillus subtilis investigated by atomic force microscopy. , 2010, Nanoscale.

[33]  Andre K. Geim,et al.  The rise of graphene. , 2007, Nature materials.

[34]  D. Rodrigues,et al.  Toxicity of a polymer-graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. , 2012, Nanoscale.

[35]  W F Heinz,et al.  Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope. , 1999, Trends in biotechnology.

[36]  J. Zimmerman,et al.  Realizing comparable oxidative and cytotoxic potential of single- and multiwalled carbon nanotubes through annealing. , 2013, Environmental science & technology.

[37]  P. Cuatrecasas,et al.  Adsorbents for affinity chromatography. Use of N-hydroxysuccinimide esters of agarose. , 1972, Biochemistry.

[38]  R. Advíncula,et al.  On the antibacterial mechanism of graphene oxide (GO) Langmuir-Blodgett films. , 2015, Chemical communications.

[39]  Mukul M. Sharma,et al.  Adhesion Forces between E. c oli Bacteria and Biomaterial Surfaces , 1999 .

[40]  G. Georgiou,et al.  Molecular determinants of bacterial adhesion monitored by atomic force microscopy. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  I. Aksay,et al.  Graphene materials and their use in dye-sensitized solar cells. , 2014, Chemical reviews.

[42]  Omid Akhavan,et al.  Toxicity of graphene and graphene oxide nanowalls against bacteria. , 2010, ACS nano.

[43]  Nelson Durán,et al.  Nanotoxicity of graphene and graphene oxide. , 2014, Chemical research in toxicology.

[44]  Jae Woong Han,et al.  Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa , 2012, International journal of nanomedicine.

[45]  J. White,et al.  Graphene in the aquatic environment: adsorption, dispersion, toxicity and transformation. , 2014, Environmental science & technology.

[46]  Haiping Fang,et al.  Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. , 2013, Nature nanotechnology.

[47]  Menachem Elimelech,et al.  Influence of Growth Phase on Adhesion Kinetics of Escherichia coli D21g , 2005, Applied and Environmental Microbiology.

[48]  Menachem Elimelech,et al.  Electronic-structure-dependent bacterial cytotoxicity of single-walled carbon nanotubes. , 2010, ACS nano.

[49]  Baoxia Mi,et al.  Graphene Oxide Membranes for Ionic and Molecular Sieving , 2014, Science.