Abstract
There is a growing demand for silver-based biocides, including both ionic silver forms and metallic nanosilver. The use of metallic nanosilver, typically chemically produced, faces challenges including particle agglomeration, high costs, and upscaling difficulties . Additionally, there exists a need for the development of a more eco-friendly production of nanosilver. In this study, Gram-positive and Gram-negative bacteria were utilized in the non-enzymatic production of silver nanoparticles via the interaction of silver ions and organic compounds present on the bacterial cell. Only lactic acid bacteria, Lactobacillus spp., Pediococcus pentosaceus, Enterococcus faecium, and Lactococcus garvieae, were able to reduce silver. The nanoparticles of the five best producing Lactobacillus spp. were examined more into detail with transmission electron microscopy. Particle localization inside the cell, the mean particle size, and size distribution were species dependent, with Lactobacillus fermentum having the smallest mean particle size of 11.2 nm, the most narrow size distribution, and most nanoparticles associated with the outside of the cells. Furthermore, influence of pH on the reduction process was investigated. With increasing pH, silver recovery increased as well as the reduction rate as indicated by UV–VIS analyses. This study demonstrated that Lactobacillus spp. can be used for a rapid and efficient production of silver nanoparticles.
References
Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloid Surf B-Biointerfaces 28:313–318
Aslim B, Beyatli Y, Yuksekdag ZN (2006) Productions and monomer compositions of exopolysaccharides by Lactobacillus delbrueckii subsp bulgaricus and Streptococcus thermophilus strains isolated from traditional home-made yoghurts and raw milk. Int J Food Sci Technol 41:973–979
Atiyeh BS, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33(2):139–148
Boonaert CJP, Rouxhet PG (2000) Surface of lactic acid bacteria: relationships between chemical composition and physicochemical properties. Appl Environ Microbiol 66:2548–2554
Chen JC, Lin ZH, Ma XX (2003) Evidence of the production of silver nanoparticles via pretreatment of Phoma sp. 3.2283 with silver nitrate. Lett Appl Microbiol 37:105–108
Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 76:159–184
Duran N, Marcato PD, Alves OL, Souza GI, Esposito E (2005) Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. J Nanobiotechnol 3:8
Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, Yacaman MJ (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnol 3:6
Fu MX, Li QB, Sun DH, Lu YH, He N, Deng X, Wang HX, Huang JL (2006) Rapid preparation process of silver nanoparticles by bioreduction and their characterizations. Chin J Chem Eng 14:114–117
Fuller SB, Wilhelm EJ, Jacobson JA (2002) Ink-jet printed nanoparticle microelectromechanical systems. J Microelectromech Syst 11:54–60
Jolly L, Vincent SJF, Duboc P, Nesser JR (2002) Exploiting exopolysaccharides from lactic acid bacteria. Antonie Van Leeuwenhoek 82:367–374
Kalimuthu K, Babu RS, Venkataraman D, Bilal M, Gurunathan S (2008) Biosynthesis of silver nanocrystals by Bacillus licheniformis. Colloid Surf B-Biointerfaces 65:150–153
Kamat PV (2002) Photophysical, photochemical and photocatalytic aspects of metal nanoparticles. J Phys Chem B 106:7729–7744
Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3:95–101
Kim KJ, Sung WS, Moon SK, Choi JS, Kim JG, Lee DG (2008) Antifungal effect of silver nanoparticles on dermatophytes. J Microbiol Biotechnol 18:1482–1484
Klasen HJ (2000a) Historical review of the use of silver in the treatment of burns. I. Early uses. Burns 26:117–130
Klasen HJ (2000b) A historical review of the use of silver in the treatment of burns. II. Renewed interest for silver. Burns 26:131–138
Klaus T, Joerger R, Olsson E, Granqvist CG (1999) Silver-based crystalline nanoparticles, microbially fabricated. Proc Natl Acad Sci U S A 96:13611–13614
Kowshik M, Ashtaputre S, Kharrazi S, Vogel W, Urban J, Kulkarni SK, Paknikar KM (2003) Extracellular synthesis of silver nanoparticles by a silver-tolerant yeast strain MKY3. Nanotechnology 14:95–100
Ledwith DM, Whelan AM, Kelly JM (2007) A rapid, straight-forward method for controlling the morphology of stable silver nanoparticles. J Mater Chem 17:2459–2464
Lin ZY, Zhou CH, Wu JM, Zhou JZ, Wang L (2005) A further insight into the mechanism of Ag + biosorption by Lactobacillus sp strain A09. Spectrochim Acta Part A-Mol Biomol Spectrosc 61:1195–1200
Lu L, Sun RWY, Chen R, Hui CK, Ho CM, Luk JM, Lau GKK, Che CM (2008) Silver nanoparticles inhibit hepatitis B virus replication. Antivir Ther 13:253–262
Mast J, Nanbru C, van den Berg T, Meulemans G (2005) Ultrastructural changes of the tracheal epithelium after vaccination of day-old chickens with the La Sota strain of Newcastle disease virus. Vet Pathol 42:559–565
Medina F, Chimentao RJ, Kirm I, Rodriguez X, Cesteros Y, Salagre P, Sueiras JE, Fierro JLG (2005) Sensitivity of styrene oxidation reaction to the catalyst structure of silver nanoparticles. Appl Surf Sci 252:793–800
Merroun M, Rossberg A, Hennig C, Scheinost AC, Selenska-Pobell S (2007) Spectroscopic characterization of gold nanoparticles formed by cells and S-layer protein of Bacillus sphaericus JG-A12. Mater Sci Eng C-Biomim Supramol Syst 27:188–192
Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR, Khan MI, Parishcha R, Ajaykumar PV, Alam M, Kumar R, Sastry M (2001) Fungus-mediated synthesis of silver nanoparticles and their immobilization in the lycelial matrix: a novel biological approach to nanoparticle synthesis. Nanoletters 1:515–519
Nair B, Pradeep T (2002) Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus strains. Cryst Growth Des 2:293–298
Panacek A, Kvitek L, Prucek R, Kolar M, Vecerova R, Pizurova N, Sharma VK, Nevecna T, Zboril R (2006) Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 110:16248–16253
Rao CNR, Cheetham AK (2001) Science and technology of nanomaterials: current status and future prospects. J Mater Chem 11:2887–2894
Sadowski Z, Maliszewska I, Polowczyk I, Kozlecki T, Grochowalska B (2008) Biosynthesis of colloidal-silver particles using microorganisms. Pol J Chem 82:377–382
Sastry M, Ahmad A, Khan MI, Kumar R (2003) Biosynthesis of metal nanoparticles using fungi and actinomycete. Curr Sci 85:162–170
Shahverdi AR, Minaeian S, Shahverdi HR, Jamalifar H, Nohi AA (2007) Rapid synthesis of silver nanoparticles using culture supernatants of Enterobacteria: a novel biological approach. Process Biochem 42:919–923
Silver S, Phung LT, Silver G (2006) Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol 33:627–634
Tavakoli A, Sohrabi M, Kargari A (2007) A review of methods for synthesis of nanostructured metals with emphasis on iron compounds. Chem Pap 61:151–170
Tilaki RM, Zad AI, Mahdavi SM (2006) Stability, size and optical properties of silver nanoparticles prepared by laser ablation in different carrier media. Appl Phys A-Mater Sci Process 84:215–219
van Hullebusch E, Zandvoort M, Lens P (2003) Metal immobilisation by biofilms: mechanisms and analytical tools. Rev Environ Sci Biotechnol 2:9–33
Vigneshwaran N, Ashtaputre NM, Varadarajan PV, Nachane RP, Paralikar KM, Balasubramanya RH (2007) Biological synthesis of silver nanoparticles using the fungus Aspergillus flavus. Mater Lett 61:1413–1418
Zhang HR, Li QB, Lu YH, Sun DH, Lin XP, Deng X, He N, Zheng SZ (2005) Biosorption and bioreduction of diamine silver complex by Corynebacterium. J Chem Technol Biotechnol 80:285–290
Zhang HR, Li QB, Wang HX, Sun DH, Lu YH, He N (2007) Accumulation of silver(I) ion and diamine silver complex by Aeromonas SH10 biomass. Appl Biochem Biotechnol 143:54–62
Acknowledgments
This work was supported by the project grant 71333 of IWT, the Institute for the Promotion of Innovation by Science and Technology in Flanders, and by the “Industrieel Onderzoeksfonds” of Ghent University (IOF07/VAL/006). We thank Niels D’ Haese and Greet Van De Velde for their assistance in the lab; Kim Verbeken for using the AAS; Olivier Janssens of the department of Solid State Sciences at Ghent University for the XRD analyses; Bart Declercq for his help with the statistics; and Brian Laird, Pieter Van De Caveye, Pieter Verhagen, and Tom Hennebel for critically reading the manuscript.
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The particle size distribution curves showing the frequency (counts) and cumulative frequency (%) for L. farciminis, L. fermentum, L. plantarum LMG 24832, L. plantarum LMG 24830, and L. rhamnosus (DOC 34 kb)
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Sintubin, L., De Windt, W., Dick, J. et al. Lactic acid bacteria as reducing and capping agent for the fast and efficient production of silver nanoparticles. Appl Microbiol Biotechnol 84, 741–749 (2009). https://doi.org/10.1007/s00253-009-2032-6
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DOI: https://doi.org/10.1007/s00253-009-2032-6