We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Skip to main content
Log in

Exopolysaccharide-mediated silver nanoparticles produced by Lactobacillus brevis NM101-1 as antibiotic adjuvant

  • Experimental Articles
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

A green, simple and effective approach was performed to synthesize potent silver nanoparticles using bacterial exopolysaccharide as both a reducing and stabilizing agent. The formation of nanoparticles was first screened by measuring the surface plasmon resonance peak around 400 nm using UV-vis spectroscopy. The morphology of the synthesized AgNPs was determined using TEM, which indicated that the AgNPs were spherical in shape and with an average size of 11–25 nm. The presence of elemental silver of the AgNPs was confirmed by EDX analysis. The possible functional groups of EPS responsible for the reduction and stabilization of AgNPs were evaluated using FTIR. The EPS reduced AgNPs showed excellent antibacterial, and antibiofilm activities against various human pathogenic bacteria. In addition, the efficiency of AgNPs with various broad-spectrum antibiotics against the tested strains was evaluated. It is evident that, the antibacterial and antibiofilm activities of the selected antibiotics were increased in the presence of AgNPs. The increase in activity was more pronounced for gram-negative bacteria Pseudomonas aeruginosa and E. coli. Interestingly, the combination of antibiotics with AgNPs has significantly increased the membrane protein leakage and ROS generation than antibiotics or AgNPs alone. This work supports that AgNPs can be used to enhance the activity of existing antibiotics against gram-negative and gram-positive bacteria for the treatment of infectious diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

References

  • Abdel-Mohsen, A.M., Hrdina, R., Burgert, L., Abdel-Rahman, R.M., Hasova, M., Smejkalova, D., Kolar, M., Pekar, M., and Aly, A.S., Antibacterial activity and cell viability of hyaluronan fiber with silver nanoparticles, Carbohydr. Polym., 2013, vol. 92, pp. 1177–1187.

    Article  CAS  PubMed  Google Scholar 

  • Akhavan, O. and Ghaderi, E., Bactericidal effects of Ag nanoparticles immobilized on surface of SiO2 thin film with high concentration, Curr. Appl. Phys., 2009, vol. 9, pp. 1381–1385.

    Article  Google Scholar 

  • Ansari, M.A., Maayah, Z.H., Bakheet, S.A., El-Kadi, A.O., and Korashy, H.M., The role of aryl hydrocarbon receptor signaling pathway in cardiotoxicity of acute lead intoxication in vivo and in vitro rat model, Toxicology, 2013, vol. 306, pp. 40–49.

    Article  CAS  PubMed  Google Scholar 

  • Balamurugan, A., Balossier, G., Laurent-Maquin, D., Pina, S., Rebelo, A.H., Faure, J., and Ferreira, J.M., An in vitro biological and anti-bacterial study on a sol–gel derived silver-incorporated bioglass system, Acad. Dental Mater., 2008, vol. 24, pp. 1343–1351.

    Article  CAS  Google Scholar 

  • Bankura, K.P., Maity, D., Mollick, M.M.R., Mondal, D., Bhowmick, B., and Bain, M.K., Synthesis, characterization and antimicrobial activity of dextran stabilized silver nanoparticles in aqueous medium, Carbohydr. Polym., 2012, vol. 89, pp. 1159–1165.

    Article  CAS  PubMed  Google Scholar 

  • Bindhu, M.R. and Umadevi, M., Synthesis of monodispersed silver nanoparticles using Hibiscus cannabinus leaf extract and its antimicrobial activity, Spectrochim. Acta A Mol. Biomol. Spectrosc., 2013, vol. 101, pp. 184–190.

    Article  CAS  PubMed  Google Scholar 

  • Chaudhari, P.R., Masurkar, S.A., Shidore, V.B., and Kamble, S.P., Effect of biosynthesized silver nanoparticles on Staphylococcus aureus biofilm quenching and prevention of biofilm formation, Nano. Micro. Lett., 2012, vol. 4, pp. 34–39.

    Article  Google Scholar 

  • Chauhan, R., Kumar, A., and Abraham, J., A biological approach to the synthesis of silver nanoparticles with Streptomyces sp. JAR1 and its antimicrobial activity, Sci. Pharm., 2013, vol. 81, pp. 607–621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, X. and Schluesener, H.J., Nanosilver: a nanoproduct in medical application, Toxicol. Lett., 2008, vol. 176, pp. 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Dar, M.A., Ingle, A., and Rai, M., Enhanced antimicrobial activity of silver nanoparticles synthesized by Cryphonectria sp. evaluated singly and in combination with antibiotics, Nanotechnol. Biol. Med., 2013, vol. 9, pp. 105–110.

    Article  CAS  Google Scholar 

  • Emerich, D.F. and Thanos, C.G., The pinpoint promise of nanoparticle-based drug delivery and molecular diagnosis, Biomol. Eng., 2006, vol. 23, pp. 171–184.

    Article  CAS  PubMed  Google Scholar 

  • Fayaz, A.M., Balaji, K., Girilal, M., Yadav, R., Kalaichelvan, P.T., and Venketesan, R., Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against Gram-positive and Gram-negative bacteria, Nanomed. Nanotechnol., 2010, vol. 6, pp. 103–109.

    Article  CAS  Google Scholar 

  • Gnanadhas, D.P., Ben Thomas, M., Thomas, R., Raichur, A.M., and Chakravortty, D., Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo, Antimicrob. Agents Chemother., 2013, vol. 57, pp. 4945–4955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gurunathan, S., Raman, J., Malek, S.N., John, P., and Vikineswary, S., Green synthesis of silver nanoparticles using Ganoderma neojaponicum Imazeki: a potential cytotoxic agent against breast cancer cells, Int. J. Nanomed., 2014, vol. 8, pp. 4399–4413.

    Google Scholar 

  • Guzmán, M.G., Dille, J., and Godet, S., Synthesis of silver nanoparticles by chemical reduction method and their antibacterial activity, Int. J. Chem. Biomol. Eng., 2009, vol. 2, pp. 171–179.

    Google Scholar 

  • Hebeish, A., Hashem, M., Abd El-Hady, M.M., and Sharaf, S., Development of CMC hydro-gels loaded with silver nanoparticles for medical applications, Carbohydr. Poly., 2013, vol. 92, pp. 407–413.

    Article  CAS  Google Scholar 

  • Hwang, I.S., Hwang, J.H., Choi, H., Kim, K.J., and Lee, D.G., Synergistic effects between silver nanoparticles and antibiotics and the mechanisms involved, J. Med. Microbiol., 2012, vol. 61, pp. 1719–1726.

    Article  CAS  PubMed  Google Scholar 

  • Inphonlek, S., Pimpha, N., and Sunintaboon, P., Synthesis of poly(methyl methacrylate) core/chitosan-mixed-polyethyleneimine shell nanoparticles and their antibacterial property, Colloids Surf. B: Biointerfaces, 2010, vol. 77, pp. 219–226.

    Article  CAS  PubMed  Google Scholar 

  • Jung, S.W., Jeong, J.I., and Kim, S.H., Characterization of hydrophobized pullulan with various hydrophobicities, Int. J. Pharm., 2003, vol. 254, pp. 109–121.

    Article  CAS  PubMed  Google Scholar 

  • Kalimuthu, K., Suresh Babu, R., Venkataraman, D., Bilal, M., and Gurunathan, S., Biosynthesis of silver nanocrystals by Bacillus licheniformis, Colloids Surf. B: Biointerfaces, 2008, vol. 65, pp. 150–153.

    Article  CAS  PubMed  Google Scholar 

  • Kalishwaralal, K., Barath, M. S., Pandian, S.R., Deepak, V., and Gurunathan, S., Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis, Colloids Surf. B: Biointerfaces, 2010, vol. 79, pp. 340–344.

    Article  CAS  PubMed  Google Scholar 

  • Kanmani, P. and Lim, S., Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens, Process Biochem., 2013, vol. 48, pp. 1099–1106.

    Article  CAS  Google Scholar 

  • Kanmani, P., Satish Kumar, R., Yuvaraj, N., Paari, K.A., Pattukumar, V., and Arul, V., Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro, Biores. Technol., 2011, vol. 102, pp. 4827–33.

    Article  CAS  Google Scholar 

  • Kim, S.H., Lee, H.S., Ruy, D.S., Choi, S.J., and Lee, D.S., Antibacterial activity of silver nanoparticles against Staphylococcus aureus and Escherichia coli, Kor. J. Microbiol. Biotechnol., 2011, vol. 39, pp. 77–85.

    CAS  Google Scholar 

  • Kora, A.J. and Rastogi, L., Enhancement of antibacterial activity of capped silver nanoparticles in combination with antibiotics, on model Gram-negative and Gram-positive bacteria, Bioinorg. Chem. Appl., 2013, vol. 5, pp. 1–7.

    Article  Google Scholar 

  • Kye, I.S., Jeon, Y.S., No, J.K., Kim, Y.J., Lee, K. H., Shin, K. H., Kim, J., Yokozawa, T., and Chung, H.Y., Reactive oxygen scavenging activity of green tea polyphenols, J. Korea Gerontol., 1999, vol. 9, pp. 10–17.

    Google Scholar 

  • Lowry, O.H., Rosebrough, N., Farr, A.L., and Randall R.J., Protein measurement with Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, pp. 265–275.

    CAS  PubMed  Google Scholar 

  • Magana, S.M., Quintana, P., Aguilar, D.H., Toledo, J.A., Angeles-Chavez, C., Cortes, M.A., Leon, L., Freile-Pelegrin, Y., and Lopez, T., Antibacterial activity of montmorillonites modified with silver, J. Mol. Catal. A: Chem., 2008, vol. 281, pp. 192–199.

    Article  CAS  Google Scholar 

  • Malik, M.A., Brien, P., and Revaprasadu, N., A simple route to the synthesis of core/shell nanoparticles of chalcogenides, Chem. Mater., 2002, vol. 14, pp. 2004–2010.

    Article  CAS  Google Scholar 

  • Mohanty, S., Mishra, S., Jena, P., Jacob, B., Sarkar, B., and Sonawane, A., An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles, Nanomed. Nanotechnol. Biol. Med., 2012, vol. 8, pp. 916–924.

    Article  CAS  Google Scholar 

  • Morones-Ramirez, J.R., Winkler, J.A., Spina, C.S., and Collins, J.J., Silver enhances antibiotic activity against gram-negative bacteria, Sci. Trans. Med., 2013, vol. 5, pp. 181–190.

    Article  Google Scholar 

  • Murdock, R.C., Braydich-Stolle, L., Schrand, A.M., Schlager, J.J., and Hussain, S.M., Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique, Toxicol. Sci., 2008, vol. 101, pp. 239–253.

    Article  CAS  PubMed  Google Scholar 

  • Nel, A., Xia, T., Madler, L., and Li, N., Toxic potential of materials at the nanolevel, Science, 2006, vol. 311, pp. 622–627.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, S., Goswami, G.K., and Nanda, K.K., Green synthesis of biopolymer–silver nanoparticle nanocomposite: An optical sensor for ammonia detection, Int. J. Biol. Macromol., 2012, vol. 51, pp. 583–589.

    Article  CAS  PubMed  Google Scholar 

  • Pandian, S.R., Deepak, V., Kalishwaralal, K., Viswanathan, P., and Gurunathan, S., Mechanism of bactericidal activity of silver nitrate—a concentration dependent bifunctional molecule, Braz. J. Microbiol., 2010, vol. 41, pp. 805–809.

    Article  CAS  Google Scholar 

  • Priyadarshini, S., Gopinath, V., Meera Priyadharsshini, N., Mubarak Ali, D., and Velusamy, P., Synthesis of anisotropic silver nanoparticles using novel strain, Bacillus flexus and its biomedical application, Coll. Sur. B: Bioint., 2013, vol. 102, pp. 232–237.

    Article  CAS  Google Scholar 

  • Rushdy, A.A. and Gomaa, E.Z., Antimicrobial compounds produced by probiotic Lactobacillus brevis isolated from dairy products, Ann. Microbiol., 2013, vol. 63, pp. 81–90.

    Article  CAS  Google Scholar 

  • Santander-Ortega, M.J., de la Fuente, M., Lozano, M.V., Bekheet, M.E., Progatzky, F., and Elouzi, A., Hydration forces as a tool for the optimization of core–shell nanoparticle vectors for cancer gene therapy, Soft Matter, 2012, vol. 8, pp. 12080–12092.

    Article  CAS  Google Scholar 

  • Shahverdi, A.R., Fakhimi, A., Shahverdi, H.R., and Minaian, S., Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli, Nanomed. Nanotechnol., 2007, vol. 3, pp. 168–171.

    Article  CAS  Google Scholar 

  • Sharma, V.K., Yngard, R.A., and Lin, Y., Silver nanoparticles: Green synthesis and their antimicrobial activities, Adv. Colloid Int. Sci., 2009, vol. 145, pp. 83–96.

    Article  CAS  Google Scholar 

  • Sondi, I. and Salopek-Sondi, B., Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria, J. Colloid Int. Sci., 2004, vol. 275, pp. 177–182.

    Article  CAS  Google Scholar 

  • Sriram, M.I., Kanth, S.B., Kalishwaralal, K., and Gurunathan, S., Antitumor activity of silver nanoparticles in Dalton’s lymphoma ascites tumor model, Int. J. Nanomed., 2010, vol. 5, pp. 753–762.

    CAS  Google Scholar 

  • Stensberg, M.C., Wei, Q.S., McLamore, E.S., Porterfield, D.M., Wei, A., and Sepulveda, M.S., Toxicological studies on silver nanoparticles: challenges and opportunities in assessment, monitoring and imaging, Nanomedicine, 2011, vol. 6, pp. 879–898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su, H.L., Chou, C.C., Hung, D.J., Lin, S.H., Pao, I.C., Lin, J.H., Huang, F.L., Dong, R.X., and Lin, J.J., The disruption of bacterial membrane integrity through ROS generation induced by nanohybrids of silver and clay, Biomaterials, 2009, vol. 30, pp. 5979–5987.

    Article  CAS  PubMed  Google Scholar 

  • Taubes, G., The bacteria fight back, Science, 2008, vol. 321, pp. 356–361.

    Article  CAS  PubMed  Google Scholar 

  • Tiwari, D.K., Behari, J., and Sen, P., Time and dosedependent antimicrobial potential of Ag nanoparticles synthesized by top down approach, Curr. Sci., 2008, vol. 95, pp. 647–655.

    CAS  Google Scholar 

  • Wang, J.X., Wen, L.X., Wang, Z.H., and Chen, J.F., Immobilization of silver on hollow silica nanospheres and nanotubes and their antibacterial effects, Mater. Chem. Phys., 2006, vol. 96, pp. 90–97.

    Article  CAS  Google Scholar 

  • Wei, G.X., Campagna, A.N., and Bobek, L.A., Effect of MUC7 peptides on the growth of bacteria and on Streptococcus mutans biofilm, J. Antimicrob. Chemother., 2006, vol. 57, pp. 1100–1109.

    Article  CAS  PubMed  Google Scholar 

  • Wei, X., Luo, M., Li, W., Yang, L., Liang, X., and Xu, L., Synthesis of silver nanoparticles by solar irradiation of cellfree Bacillus amyloliquefaciens extracts and AgNO3, Biores. Technol., 2012, vol. 103, pp. 273–278.

    Article  CAS  Google Scholar 

  • Yoksan, R. and Chirachanchai, S., Silver nanoparticleloaded chitosan–starch based films: fabrication and evaluation of tensile, barrier and antimicrobial properties, Mat. Sci. Engin. C, 2010, vol. 30, pp. 891–897.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Z. Gomaa.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomaa, E.Z. Exopolysaccharide-mediated silver nanoparticles produced by Lactobacillus brevis NM101-1 as antibiotic adjuvant. Microbiology 85, 207–219 (2016). https://doi.org/10.1134/S0026261716020077

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261716020077

Keywords

Navigation