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An environmentally benign antimicrobial nanoparticle based on a silver-infused lignin core

Abstract

Silver nanoparticles have antibacterial properties, but their use has been a cause for concern because they persist in the environment. Here, we show that lignin nanoparticles infused with silver ions and coated with a cationic polyelectrolyte layer form a biodegradable and green alternative to silver nanoparticles. The polyelectrolyte layer promotes the adhesion of the particles to bacterial cell membranes and, together with silver ions, can kill a broad spectrum of bacteria, including Escherichia coli, Pseudomonas aeruginosa and quaternary-amine-resistant Ralstonia sp. Ion depletion studies have shown that the bioactivity of these nanoparticles is time-limited because of the desorption of silver ions. High-throughput bioactivity screening did not reveal increased toxicity of the particles when compared to an equivalent mass of metallic silver nanoparticles or silver nitrate solution. Our results demonstrate that the application of green chemistry principles may allow the synthesis of nanoparticles with biodegradable cores that have higher antimicrobial activity and smaller environmental impact than metallic silver nanoparticles.

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Figure 1: Schematics of the general use cycle and principle of the bactericidal action of environmentally benign lignin-core nanoparticles (EbNPs) and the currently used silver nanoparticles (AgNPs).
Figure 2: Synthesis and characterization of EbNPs.
Figure 3: Quantification of CFU reduction efficiency as a function of Ag+ equivalent (mg l–1) of EbNPs and control samples on E. coli, P. aeruginosa and Ralstonia sp.
Figure 4: Heat map of the bioactivity of EbNPs-Ag+-PDAC, EbNPs, AgNO3(aq.) and AgNPs based on ToxCast mammalian cell and zebrafish embryo screening assays.

References

  1. Panáček, A. et al. Antifungal activity of silver nanoparticles against Candida spp. Biomaterials 30, 6333–6340 (2009).

    Article  Google Scholar 

  2. Lara, H., Garza-Trevino, E., Ixtepan-Turrent, L. & Singh, D. Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds. J. Nanobiotechnol. 9, 30 (2011).

    Article  CAS  Google Scholar 

  3. Sondi, I. & Salopek-Sondi, B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275, 177–182 (2004).

    Article  CAS  Google Scholar 

  4. Poole, K., Krebes, K., McNally, C. & Neshat, S. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J. Bacteriol. 175, 7363–7372 (1993).

    Article  CAS  Google Scholar 

  5. Panáček, A. et al. Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J. Phys. Chem. B 110, 16248–16253 (2006).

    Article  Google Scholar 

  6. Morones, J. R. et al. The bactericidal effect of silver nanoparticles. Nanotechnology 16, 2346–2353 (2005).

    Article  CAS  Google Scholar 

  7. Rai, M., Yadav, A. & Gade, A. Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76–83 (2009).

    Article  CAS  Google Scholar 

  8. Walser, T. et al. Persistence of engineered nanoparticles in a municipal solid-waste incineration plant. Nature Nanotech. 7, 520–524 (2012).

    Article  CAS  Google Scholar 

  9. Jeong, E. et al. Different susceptibilities of bacterial community to silver nanoparticles in wastewater treatment systems. J. Environ. Sci. Health Part A 49, 685–693 (2014).

    Article  CAS  Google Scholar 

  10. Levard, C., Hotze, E. M., Lowry, G. V. & Brown, G. E. Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ. Sci. Technol. 46, 6900–6914 (2012).

    Article  CAS  Google Scholar 

  11. Chinnapongse, S. L., MacCuspie, R. I. & Hackley, V. A. Persistence of singly dispersed silver nanoparticles in natural freshwaters, synthetic seawater, and simulated estuarine waters. Sci. Total Environ. 409, 2443–2450 (2011).

    Article  CAS  Google Scholar 

  12. Sharma, V. K., Siskova, K. M., Zboril, R. & Gardea-Torresdey, J. L. Organic-coated silver nanoparticles in biological and environmental conditions: fate, stability and toxicity. Adv. Colloid Interface Sci. 204, 15–34 (2014).

    Article  CAS  Google Scholar 

  13. Dobias, J. & Bernier-Latmani, R. Silver release from silver nanoparticles in natural waters. Environ. Sci. Technol. 47, 4140–4146 (2013).

    Article  CAS  Google Scholar 

  14. Stern, S. T. & McNeil, S. E. Nanotechnology safety concerns revisited. Toxicol. Sci. 101, 4–21 (2008).

    Article  CAS  Google Scholar 

  15. Ahamed, M., AlSalhi, M. S. & Siddiqui, M. K. J. Silver nanoparticle applications and human health. Clin. Chim. Acta 411, 1841–1848 (2010).

    Article  CAS  Google Scholar 

  16. Fabrega, J., Luoma, S. N., Tyler, C. R., Galloway, T. S. & Lead, J. R. Silver nanoparticles: behaviour and effects in the aquatic environment. Environ. Int. 37, 517–531 (2011).

    Article  CAS  Google Scholar 

  17. Justo-Hanani, R. & Dayan, T. The role of the state in regulatory policy for nanomaterials risk: analyzing the expansion of state-centric rulemaking in EU and US chemicals policies. Res. Policy 43, 169–178 (2014).

    Article  Google Scholar 

  18. Marchant, G., Sylvester, D. & Abbott, K. Risk management principles for nanotechnology. Nanoethics 2, 43–60 (2008).

    Article  Google Scholar 

  19. Anastas, P. & Eghbali, N. Green chemistry: principles and practice. Chem. Soc. Rev. 39, 301–312 (2010).

    Article  CAS  Google Scholar 

  20. Sharma, V. K., Yngard, R. A. & Lin, Y. Silver nanoparticles: green synthesis and their antimicrobial activities. Adv. Colloid Interface Sci. 145, 83–96 (2009).

    Article  CAS  Google Scholar 

  21. Kumar, A., Vemula, P. K., Ajayan, P. M. & John, G. Silver-nanoparticle-embedded antimicrobial paints based on vegetable oil. Nature Mater. 7, 236–241 (2008).

    Article  CAS  Google Scholar 

  22. Raveendran, P., Fu, J. & Wallen, S. L. Completely ‘green’ synthesis and stabilization of metal nanoparticles. J. Am. Chem. Soc. 125, 13940–13941 (2003).

    Article  CAS  Google Scholar 

  23. Xiu, Z., Zhang, Q., Puppala, H. L., Colvin, V. L. & Alvarez, P. J. J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 12, 4271–4275 (2012).

    Article  CAS  Google Scholar 

  24. Nel, A. E. et al. Understanding biophysicochemical interactions at the nano–bio interface. Nature Mater. 8, 543–557 (2009).

    Article  CAS  Google Scholar 

  25. Ge, C. et al. Towards understanding of nanoparticle–protein corona. Arch. Toxicol. 89, 519–539 (2015).

    Article  CAS  Google Scholar 

  26. Lundqvist, M. et al. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105, 14265–14270 (2008).

    Article  CAS  Google Scholar 

  27. Verma, A. & Stellacci, F. Effect of surface properties on nanoparticle–cell interactions. Small 6, 12–21 (2010).

    Article  CAS  Google Scholar 

  28. Monopoli, M. P., Aberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nature Nanotech. 7, 779–786 (2012).

    Article  CAS  Google Scholar 

  29. El Badawy, A. M. et al. Surface charge-dependent toxicity of silver nanoparticles. Environ. Sci. Technol. 45, 283–287 (2010).

    Article  Google Scholar 

  30. Sotiriou, G. A. & Pratsinis, S. E. Antibacterial activity of nanosilver ions and particles. Environ. Sci. Technol. 44, 5649–5654 (2010).

    Article  CAS  Google Scholar 

  31. Feng, Q. L. et al. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52, 662–668 (2000).

    Article  CAS  Google Scholar 

  32. Matsumura, Y., Yoshikata, K., Kunisaki, S. & Tsuchido, T. Mode of bactericidal action of silver zeolite and its comparison with that of silver nitrate. Appl. Environ. Microbiol. 69, 4278–4281 (2003).

    Article  CAS  Google Scholar 

  33. Norgren, M. & Edlund, H. Lignin: recent advances and emerging applications. Curr. Opin. Colloid Interface Sci. 19, 409–416 (2014).

    Article  CAS  Google Scholar 

  34. Duval, A. & Lawoko, M. A review on lignin-based polymeric, micro- and nano-structured materials. React. Funct. Polym. 85, 78–96 (2014).

    Article  CAS  Google Scholar 

  35. Guo, X., Zhang, S. & Shan, X.-Q. Adsorption of metal ions on lignin. J. Hazard. Mater. 151, 134–142 (2008).

    Article  CAS  Google Scholar 

  36. Harmita, H., Karthikeyan, K. G. & Pan, X. Copper and cadmium sorption onto kraft and organosolv lignins. Bioresour. Technol. 100, 6183–6191 (2009).

    Article  CAS  Google Scholar 

  37. Wege, H. A., Kim, S., Paunov, V. N., Zhong, Q. & Velev, O. D. Long-term stabilization of foams and emulsions with in-situ formed microparticles from hydrophobic cellulose. Langmuir 24, 9245–9253 (2008).

    Article  CAS  Google Scholar 

  38. Frangville, C. et al. Fabrication of environmentally biodegradable lignin nanoparticles. ChemPhysChem 13, 4235–4243 (2012).

    Article  CAS  Google Scholar 

  39. Petridis, L. et al. Self-similar multiscale structure of lignin revealed by neutron scattering and molecular dynamics simulation. Phys. Rev. E 83, 061911 (2011).

    Article  Google Scholar 

  40. Kim, S., Barraza, H. & Velev, O. D. Intense and selective coloration of foams stabilized with functionalized particles. J. Mater. Chem. 19, 7043–7049 (2009).

    Article  CAS  Google Scholar 

  41. Langsrud, S., Sundheim, G. & Borgmann-Strahsen, R. Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. J. Appl. Microbiol. 95, 874–882 (2003).

    Article  CAS  Google Scholar 

  42. Silva, T. et al. Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: comparison between general linear model-predicted and observed toxicity. Sci. Total Environ. 468–469, 968–976 (2014).

    Article  Google Scholar 

  43. Tan, S., Erol, M., Attygalle, A., Du, H. & Sukhishvili, S. Synthesis of positively charged silver nanoparticles via photoreduction of AgNO3 in branched polyethyleneimine/HEPES solutions. Langmuir 23, 9836–9843 (2007).

    Article  CAS  Google Scholar 

  44. Kavlock, R. et al. Update on EPA's ToxCast program: providing high throughput decision support tools for chemical risk management. Chem. Res. Toxicol. 25, 1287–1302 (2012).

    Article  CAS  Google Scholar 

  45. Choi, O. et al. Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res. 43, 1879–1886 (2009).

    Article  CAS  Google Scholar 

  46. Wandrey, C., Hernández-Barajas, J. & Hunkeler, D. in Radical polymerisation polyelectrolytes Vol. 145 Advances in Polymer Science (eds Capek, I. et al.) Ch. 3, 123–183 (Springer, 1999).

    Book  Google Scholar 

  47. Gélinas, P. & Goulet, J. Neutralization of the activity of eight disinfectants by organic matter. J. Appl. Bacteriol. 54, 243–247 (1983).

    Article  Google Scholar 

  48. Lundquist, K., Kirk, T. K. & Connors, W. Fungal degradation of kraft lignin and lignin sulfonates prepared from synthetic 14C-lignins. Arch. Microbiol. 112, 291–296 (1977).

    Article  CAS  Google Scholar 

  49. Bugg, T. D. H., Ahmad, M., Hardiman, E. M. & Rahmanpour, R. Pathways for degradation of lignin in bacteria and fungi. Nat. Prod. Rep. 28, 1883–1896 (2011).

    Article  CAS  Google Scholar 

  50. Klein, C. L. et al. NM-series of Representative Manufactured Nanomaterials NM-300 Silver Characterisation, Stability, Homogeneity (JRC Scientific and Technical Reports, Joint Research Centre, European Commission, 2011).

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Acknowledgements

The authors acknowledge funding from the United States Environmental Protection Agency (US EPA) via a Pathfinder Innovation Projects grant, the National Science Foundation Tringle Center for Programmable Soft Matter (DMR-1121107) and North Carolina State University. The authors thank D. Plemmons and A.K. Sarkar for assistance with initial studies, and H. Armstrong for assistance with Ag+ ion desorption studies. Thanks go to M. Moore for the analysis and characterization of PDAC-resistant Ralstonia sp. bacteria, R. Garcia for transmission electron microscopy analysis and K. Hutchinson and the Analytical Spectroscopy Service Laboratory at North Carolina State University for silver content analysis. S.D.S. acknowledges financial support from European Cooperation in Science and Technology Actions MP1305 and MP1106, as well European Union Project FP7-REGPOT-2011-1, ‘Beyond Everest’. The views expressed in this paper are those of the authors and do not necessarily represent the views or policies of the United States Environmental Protection Agency.

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Contributions

A.P.R. planned and performed the key experiments and analysed the results. J.S.B. synthesized EbNPs and tested their antimicrobial efficiency. B.B. contributed to discussions and confocal microscopy imaging. A.W., S.G., K.H., and E.A.H. carried out the EPA toxicity evaluation, and analysed and plotted the ToxCast data. A.P.R., A.W. and O.D.V. analysed the results, and all authors discussed them and commented on the manuscript. O.D.V., V.N.P. and S.D.S. conceived the project and contributed with ideas and analysis. O.D.V. is the principal investigator, and led the research team.

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Correspondence to Orlin D. Velev.

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A.P.R., V.N.P., S.D.S. and O.D.V. declare potential financial interests in the future development and commercialization of similar nanomaterials. NC State University has filed a patent application (PCT/US2014/022382) and has licensed the EbNP technology to a commercial entity.

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Richter, A., Brown, J., Bharti, B. et al. An environmentally benign antimicrobial nanoparticle based on a silver-infused lignin core. Nature Nanotech 10, 817–823 (2015). https://doi.org/10.1038/nnano.2015.141

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