Antimicrobial properties of graphene-like nanoparticles: coating effect on Staphylococcus aureus

  • M. Olivi
  • M. Alfè
  • V. Gargiulo
  • F. Valle
  • F. Mura
  • M. Di Giosia
  • S. Rapino
  • C. Palleschi
  • D. Uccelletti
  • S. Fiorito
Research Paper
First Online:
Received:
Accepted:

Abstract

The exploitation of nanomaterials with antimicrobial properties has attracted an ever-growing interest in the recent years. Carbon-based materials, such as graphene and graphene family materials (GFMs), have gained most of the attention for application in many biomedical fields. Here, we describe the antimicrobial activity of graphene-like (GL) layers derived from the chemical demolition of carbon black, against the planktonic growth of Staphylococcus aureus cells, primary cause of hospital and community-acquired infections, often leading to bacteremia and sepsis. The inhibitory capabilities of GL layers on the formation of S. aureus biofilm are also assessed. The antimicrobial properties seem based mainly on the interaction between GL layers and bacteria surfaces. FESEM and AFM analyses suggest that the GL layers coat the cells as soon as they get in contact with them, as also indicated by the wettability of the GLs.

Keywords

Graphene-like (GL) layers antimicrobial properties AFM Gram-positive 
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Notes

Acknowledgements

This work was supported by ATENEO 2013 to DU. FV thanks the National Flagship Project NANOMAX N-CHEM.

Supplementary material

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References

  1. Alfè M, Gargiulo V, Di Capua R (2015) Tuning the surface morphology of self-assembled graphene-like thin films through pH variation. Appl Surf Sci 353:628–635CrossRefGoogle Scholar
  2. Alfè M, Gargiulo V, Di Capua R, Chiarella F, Rouzaud JN, Vergara A, Ciajolo A (2012) Wet chemical method for making graphene-like films from carbon black. ACS Appl Mater Interfaces 4:4491–4498CrossRefGoogle Scholar
  3. Alfè M, Gargiulo V, Lisi L, Di Capua R (2014b) Synthesis and characterization of conductive copper-based metal-organic framework/graphene-like composites. Mater Chem Phys 147(3):744–750CrossRefGoogle Scholar
  4. Alfè M, Spasiano D, Gargiulo V, Vitiello G, Di Capua R, Marotta R (2014a) TiO2/graphene-like photocatalysts for selective oxidation of 3-pyridine-methanol to vitamin B3 under UV/solar simulatedradiation in aqueous solution at room conditions: the effect of morphology on catalyst performances. Appl Catal A-Genl 487:91–99CrossRefGoogle Scholar
  5. Ansari AM, Khan HM, Khan AA, Cameotra WS, Pal R (2013) Antibiofilm efficacy of silver nanoparticles against biofilm of extended spectrum β-lactamase isolates of Escherichia coli and Klebsiella pneumoniae. Appl Nanosci 4(7):859–868CrossRefGoogle Scholar
  6. Akhavan O, Ghaderi E, Esfandiar A (2011) Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. J Phys Chem B 15:6279–6288CrossRefGoogle Scholar
  7. Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–5736CrossRefGoogle Scholar
  8. Bao Q, Zhang D, Qi P (2011) Synthesis and characterization of silver nanoparticle and graphene oxide nanosheet composites as a bactericidal agent for water disinfection. J Colloid Interf Sci 360:463–470CrossRefGoogle Scholar
  9. Bhattacharya P, Du D, Lin Y (2014) Bioinspired nanoscale materials for biomedical and energy applications. J R Soc Interface 11:20131067CrossRefGoogle Scholar
  10. Carpio MIE, Santos CM, Wei X, Rodrigues DF (2012) Toxicity of a polymer–graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale 4(15):4746–4756CrossRefGoogle Scholar
  11. Chaibenjawong P, Foster SJ (2011) Desiccation tolerance in Staphylococcus aureus. Arch Microbiol 193(2):125–135CrossRefGoogle Scholar
  12. de Moraes AC, Lima BA, de Faria AF, Brocchi M, Alves OL (2015) Graphene oxide-silver nanocomposite as a promising biocidal agent against methicillin-resistant Staphylococcus aureus. Int J Nanomedicine 10:6847–6861CrossRefGoogle Scholar
  13. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193CrossRefGoogle Scholar
  14. Epstein AK, Pokroy B, Seminara A, Aizenberg J (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Publ Natl Acad Sci 108:995–1000CrossRefGoogle Scholar
  15. Feng Y, Chen CJ, Su LH, Hu S, Yu J, Chiu CH (2008) Evolution and pathogenesis of Staphylococcus aureus: lessons learned from genotyping and comparative genomics. FEMS Microbiol Rev 32(1):23–37CrossRefGoogle Scholar
  16. Gargiulo V, Alfè M, Di Capua R, Togna AR, Cammisotto V, Fiorito S, Musto A, Navarra A, Parisi S, Pezzella A (2015) Supplementing π-systems: eumelanin and graphene-like integration towards high conductive material for mammalian cell culture bio-interface. J Mater Chem B 3:5070CrossRefGoogle Scholar
  17. Gurunathan S, Han JW, Dayem AA, Eppakayala V, Kim JH (2012) Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomedicine 7:5901–5914CrossRefGoogle Scholar
  18. Hegaba HM, ElMekawyc A, Zoua L, Mulcahya D, Sainta CP, Ginic-Markovic M (2016) The controversial antibacterial activity of graphene-based materials. Carbon 105:362–376CrossRefGoogle Scholar
  19. Hu WB, Peng C, Luo WJ, Lv M, Li X, Li D, Huang Q, Fan C (2010) Graphene-based Antibacterical paper. ACS Nano 4:4317–4323CrossRefGoogle Scholar
  20. Huh AJ, Kwon YJ (2011) “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Control Release 156(2):128–145CrossRefGoogle Scholar
  21. Jastrzębska AM, Kurtycz P, Olszyna AR (2012) Recent advances in graphene family materials toxicity investigations. J Nanopart Res 14:1–21Google Scholar
  22. Jastrzębska AM, Olszyna AR (2015) The ecotoxicity of graphene family materials: current status, knowledge gaps and future needs. J Nanopart Res 17:40CrossRefGoogle Scholar
  23. Li J, Wang G, Zhu H, Zhang M, Zheng X, Di Z, Liu X, Wang X (2014) Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Sci Rep 4:4359Google Scholar
  24. Liu S, Zeng TH, Hofmann M, Burcombe E, Wei J, Jiang R, Kong J, Chen Y (2011) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5(9):6971–6980CrossRefGoogle Scholar
  25. Liu S, Hu Ming Z, Tingying H, Wu R, Jiang R, Wei J, Wang L, Kong J, Chen Y (2012) Lateral dimension-dependent antibacterial activity of graphene oxide sheets. Langmuir 28(33):12364–12372CrossRefGoogle Scholar
  26. Mannoor MS, Tao H, Clayton JD, Sengupta A, Kaplan DL, Naik RR, Verma N, Omenetto FG, McAlpine MC (2012) Graphene-based wireless bacteria detection on tooth enamel. Nat Commun 3:763CrossRefGoogle Scholar
  27. Nečas D, Klapetek P (2012) Gwyddion: an open-source software for SPM data analysis. Cent Eur J Phys 10(1):181–188Google Scholar
  28. Olivi M, Zanni E, De Bellis G, Talora C, Sarto MS, Palleschi C, Flahaut E, Monthioux M, Rapino S, Uccelletti D, Fiorito S (2013) Inhibition of microbial growth by carbon nanotube networks. Nanoscale 5:9023CrossRefGoogle Scholar
  29. Parra C, Dorta F, Jimenez E, Henríquez R, Ramírez C, Rojas R, Villalobos P (2015) A nanomolecular approach to decrease adhesion of biofouling-producing bacteria to graphene-coated material. J Nanobiotechnology 16:13–82Google Scholar
  30. Perreault F, de Faria AF, Nejati S, Elimelech M (2015) Antimicrobial properties of graphene oxide nanosheets: why size matters. ACS Nano 9:7226–7236CrossRefGoogle Scholar
  31. Rizzo AKLY, Theek B, Storm G, Kiessling F, Lammers L (2013) Recent progress in nanomedicine: therapeutic, diagnostic and theranostic applications. Curr Opin Biotechnol 24:1159–1166CrossRefGoogle Scholar
  32. Salas EC, Sun Z, Luttge A, Tour JM (2010) Reduction of graphene oxide via bacterial respiration. ACS Nano 4:4852–4856CrossRefGoogle Scholar
  33. Sakai H, Procop GW, Kobayashi N, Togawa D, Wilson DA, Borden L, Krebs V, Bauer TW (2004) Simultaneous detection of Staphylococcus aureus and coagulase-negative staphylococci in positive blood cultures by real-time PCR with two fluorescence resonance energy transfer probe sets. J Clin Microbiol 42(12):5739–5744CrossRefGoogle Scholar
  34. Santos CM, Tria MCR, Vergara RAMV, Ahmed F, Advincula RC, Rodrigues DF (2011) Antimicrobial graphene polymer (PVK-GO) nanocomposite films. Chem Comm 47(31):8892–8894CrossRefGoogle Scholar
  35. Shi L, Günther S, Hübschmann T, Wick LY, Harms H, Müller S (2007) Limits of propidium iodide as a cell viability indicator for environmental bacteria. Cytom Part A 71(8):592–598CrossRefGoogle Scholar
  36. Taylor E, Webster TJ (2011) Reducing infections through nanotechnology and nanoparticles. Int J Nanomedicine 6:1463–1473CrossRefGoogle Scholar
  37. Tu Y, Lv M, Xiu P, Huynh T, Zhang M, Castelli M, Liu Z, Huang Q, Fan C, Fang H, Zhou R (2013) Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nat Nanotechnol 8:594–601CrossRefGoogle Scholar
  38. Wu MC, Deokar AR, Liao JH, Shih PY, Ling YC (2013) Graphene-based photothermal agent for rapid and effective killing of bacteria. ACS Nano 7:1281–1290CrossRefGoogle Scholar
  39. Yang K, Li Y, Tan X, Peng R, Liu Z (2012) Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small 9(9–10):1492–1503Google Scholar
  40. Zanni E, Bracciale GMP, Broggi A, Santarelli ML, Sarto MS, Palleschi C, Uccelletti D (2012) Graphite nanoplatelets and Caenorhabditis elegans: insights from an in vivo model. Nano Lett 12(6):2740–2744CrossRefGoogle Scholar
  41. Zhu ZJ, Su M, Ma L, Liu DJ, Wang ZX (2013) Preparation of graphene oxide–silver nanoparticle nanohybrids with highly antibacterial capability. Talanta 117:449–455CrossRefGoogle Scholar
  42. Zu SZ, Han BH (2009) Aqueous dispersion of graphene sheets stabilized by Pluronic copolymers: formation of Supramolecular hydrogel. J Phys Chem C 113:13651–13657CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Biology and BiotechnologySapienza University of RomeRomeItaly
  2. 2.Institute for Research on CombustionCNRNaplesItaly
  3. 3.Institute of Nanostructured MaterialsISMNBolognaItaly
  4. 4.Department of ChemistrySapienza University of RomeRomeItaly
  5. 5.Department of Chemistry “Giacomo Ciamician”University of BolognaBolognaItaly
  6. 6.Institute of Translational PharmacologyCNRRomeItaly

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