Abstract
Faceted silver nanostructures including triangular nanoprisms, nanotetrahedra, and nanodecahedra were synthesized via a facile photochemical method at controlled wavelengths using spherical nanoparticles as the seeds. Scanning transmission electron microscopy studies showed that the resulting nanostructures were much larger in size (20–50 nm) than the spherical seed nanoparticles (under 5 nm), and X-ray diffraction as well as high-resolution transmission electron microscopy measurements confirmed that these nanostructures exhibited predominantly {111} faceted surfaces. Importantly, the silver nanostructures demonstrated markedly better antimicrobial activity than the spherical seed nanoparticles as evidenced by a lower minimum inhibitory concentration and more dramatic changes in both growth rate and lag phase at lower concentrations, which were attributed to the greater reactivity of the {111} faceted surfaces toward oxygen-rich bacterial surface moieties that allowed for more rapid localization to bacterial cells and increased interactions with structurally vital outer-membrane proteins. These results highlight the significance of surface morphologies of metal nanostructures in the manipulation of their antimicrobial activity.
Similar content being viewed by others
References
Alexander JW (2009) History of the medical use of silver. Surg Infect (Larchmt) 10(3):289–292. doi:10.1089/sur.2008.9941
Russell AD, Hugo WB (1994) Antimicrobial activity and action of silver. Prog Med Chem 31:351–370
Maillard JY, Hartemann P (2013) Silver as an antimicrobial: facts and gaps in knowledge. Crit Rev Microbiol 39(4):373–383. doi:10.3109/1040841X.2012.713323
Marambio-Jones C, Hoek EMV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12(5):1531–1551. doi:10.1007/s11051-010-9900-y
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(1):95–101. doi:10.1016/j.nano.2006.12.001
Xu FF, Imlay JA (2012) Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl Environ Microbiol 78(10):3614–3621. doi:10.1128/AEM.07368-11
Liau SY, Read DC, Pugh WJ, Furr JR, Russell AD (1997) Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 25(4):279–283
Holt KB, Bard AJ (2005) Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag+. Biochemistry 44(39):13214–13223. doi:10.1021/bi0508542
Petering HG (1976) Pharmacology and toxicology of heavy-metals—Silver. Pharmacol Ther Pt A 1(2):127–130. doi:10.1016/0362-5478(76)90002-4
Schreurs WJ, Rosenberg H (1982) Effect of silver ions on transport and retention of phosphate by Escherichia coli. J Bacteriol 152(1):7–13
Yamane T, Davidson N (1962) On the complexing of deoxyribonucleic acid by silver (I). Biochim Biophys Acta 55:609–621
Kvitek L, Panacek A, Soukupova J, Kolar M, Vecerova R, Prucek R, Holecova M, Zboril R (2008) Effect of surfactants and polymers on stability and antibacterial activity of silver nanoparticles (NPs). J Phys Chem C 112(15):5825–5834. doi:10.1021/Jp711616v
Raffi M, Hussain F, Bhatti TM, Akhter JI, Hameed A, Hasan MM (2008) Antibacterial characterization of silver nanoparticles against E. coli ATCC-15224. J Mater Sci Technol 24(2):192–196
Smetana AB, Klabunde KJ, Marchin GR, Sorensen CM (2008) Biocidal activity of nanocrystalline silver powders and particles. Langmuir 24(14):7457–7464. doi:10.1021/la800091y
Vertelov GK, Krutyakov YA, Efremenkova OV, Olenin AY, Lisichkin GV (2008) A versatile synthesis of highly bactericidal Myramistin(R) stabilized silver nanoparticles. Nanotechnology 19(35):355707. doi:10.1088/0957-4484/19/35/355707
Porel S, Ramakrishna D, Hariprasad E, Gupta AD, Radhakrishnan TP (2011) Polymer thin film with in situ synthesized silver nanoparticles as a potent reusable bactericide. Curr Sci India 101(7):927–934
Jones SA, Bowler PG, Walker M, Parsons D (2004) Controlling wound bioburden with a novel silver-containing Hydrofiber dressing. Wound Repair Regen 12(3):288–294. doi:10.1111/j.1067-1927.2004.012304.x
Leaper DJ (2006) Silver dressings: their role in wound management. Int Wound J 3(4):282–294. doi:10.1111/j.1742-481X.2006.00265.x
Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16(10):2346–2353. doi:10.1088/0957-4484/16/10/059
Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73(6):1712–1720. doi:10.1128/AEM.02218-06
Horswell SL, Pinheiro AL, Savinova ER, Danckwerts M, Pettinger B, Zei MS, Ertl G (2004) A comparative study of hydroxide adsorption on the (111), (110), and (100) faces of silver with cyclic voltammetry, ex situ electron diffraction, and in situ second harmonic generation. Langmuir 20(25):10970–10981. doi:10.1021/la0483818
Jin R, Cao Y, Mirkin CA, Kelly KL, Schatz GC, Zheng JG (2001) Photoinduced conversion of silver nanospheres to nanoprisms. Science 294(5548):1901–1903. doi:10.1126/science.1066541
Thrall ES, Steinberg AP, Wu XM, Brus LE (2013) The role of photon energy and semiconductor substrate in the plasmon-mediated photooxidation of citrate by silver nanoparticles. J Phys Chem C 117(49):26238–26247. doi:10.1021/Jp409586z
Xue C, Metraux GS, Millstone JE, Mirkin CA (2008) Mechanistic study of photomediated triangular silver nanoprism growth. J Am Chem Soc 130(26):8337–8344. doi:10.1021/ja8005258
Lu HF, Zhang HX, Yu X, Zeng SW, Yong KT, Ho HP (2012) Seed-mediated Plasmon-driven Regrowth of Silver Nanodecahedrons (NDs). Plasmonics 7(1):167–173. doi:10.1007/s11468-011-9290-8
Pastoriza-Santos I, Liz-Marzan LM (2008) Colloidal silver nanoplates. State of the art and future challenges. J Mater Chem 18(15):1724–1737. doi:10.1039/B716538b
Jin R, Cao YC, Hao E, Metraux GS, Schatz GC, Mirkin CA (2003) Controlling anisotropic nanoparticle growth through plasmon excitation. Nature 425(6957):487–490. doi:10.1038/nature02020
Millstone JE, Hurst SJ, Metraux GS, Cutler JI, Mirkin CA (2009) Colloidal gold and silver triangular nanoprisms. Small 5(6):646–664. doi:10.1002/smll.200801480
Callegari A, Tonti D, Chergui M (2003) Photochemically grown silver nanoparticles with wavelength-controlled size and shape. Nano Lett 3(11):1565–1568. doi:10.1021/nl034757a
Bastys V, Pastoriza-Santos I, Rodriguez-Gonzalez B, Vaisnoras R, Liz-Marzan LM (2006) Formation of silver nanoprisms with surface plasmons at communication wavelengths. Adv Funct Mater 16(6):766–773
Khan MAM, Kumar S, Ahamed M, Alrokayan SA, AlSalhi MS (2011) Structural and thermal studies of silver nanoparticles and electrical transport study of their thin films. Nanoscale Res Lett 6. Artn 434. doi:10.1186/1556-276x-6-434
Liu T, Li DS, Yang DR, Jiang MH (2011) Preparation of echinus-like SiO2@Ag structures with the aid of the HCP phase. Chem Commun 47(18):5169–5171. doi:10.1039/C1cc10401b
McEachran M, Kitaev V (2008) Direct structural transformation of silver platelets into right bipyramids and twinned cube nanoparticles: morphology governed by defects. Chem Commun (Camb) 44:5737–5739. doi:10.1039/b813519c
Gao Y, Jiang P, Song L, Wang JX, Liu LF, Liu DF, Xiang YJ, Zhang ZX, Zhao XW, Dou XY, Luo SD, Zhou WY, Xie SS (2006) Studies on silver nanodecahedrons synthesized by PVP-assisted N, N-dimethylformamide (DMF) reduction. J Crystal Growth 289(1):376–380. doi:10.1016/j.jcrysgro.2005.11.123
Zhang J, Li S, Wu J, Schatz GC, Mirkin CA (2009) Plasmon-mediated synthesis of silver triangular bipyramids. Angew Chem Int Ed Engl 48(42):7787–7791. doi:10.1002/anie.200903380
Wiley BJ, Xiong Y, Li ZY, Yin Y, Xia Y (2006) Right bipyramids of silver: a new shape derived from single twinned seeds. Nano Lett 6(4):765–768. doi:10.1021/nl060069q
Pietrobon B, Kitaev V (2008) Photochemical synthesis of monodisperse size-controlled silver decahedral nanoparticles and their remarkable optical properties. Chem Mater 20(16):5186–5190. doi:10.1021/Cm800926u
Zheng X, Zhao X, Guo D, Tang B, Xu S, Zhao B, Xu W, Lombardi JR (2009) Photochemical formation of silver nanodecahedra: structural selection by the excitation wavelength. Langmuir 25(6):3802–3807. doi:10.1021/la803814j
Rocha TCR, Zanchet D (2007) Structural defects and their role in the growth of Ag triangular nanoplates. J Phys Chem C 111(19):6989–6993. doi:10.1021/Jp0702696
Zhou J, An J, Tang B, Xu S, Cao Y, Zhao B, Xu W, Chang J, Lombardi JR (2008) Growth of tetrahedral silver nanocrystals in aqueous solution and their SERS enhancement. Langmuir 24(18):10407–10413. doi:10.1021/la800961j
Germain V, Li J, Ingert D, Wang ZL, Pileni MP (2003) Stacking faults in formation of silver nanodisks. J Phys Chem B 107(34):8717–8720
Aherne D, Ledwith DM, Gara M, Kelly JM (2008) Optical properties and growth aspects of silver nanoprisms produced by a highly reproducible and rapid synthesis at room temperature. Adv Funct Mater 18(14):2005–2016. doi:10.1002/adfm.200800233
Creighton JA, Eadon DG (1991) Ultraviolet visible absorption-spectra of the colloidal metallic elements. J Chem Soc Faraday Trans 87(24):3881–3891
Kelly KL, Coronado E, Zhao LL, Schatz GC (2003) The optical properties of metal nanoparticles: the influence of size, shape, and dielectric environment. J Phys Chem B 107(3):668–677. doi:10.1021/Jp026731y
Xu S, Tang B, Zheng X, Zhou J, An J, Ning X, Xu W (2009) The facet selectivity of inorganic ions on silver nanocrystals in etching reactions. Nanotechnology 20(41):415601. doi:10.1088/0957-4484/20/41/415601
Gutierrez M, Henglein A (1993) Formation of colloidal silver by push-pull reduction of Ag+. J Phys Chem 97(44):11368–11370. doi:10.1021/J100146a003
Jiang ZJ, Liu CY, Li YJ (2004) Electrochemical studies of silver nanoparticles tethered on silica sphere. Chem Lett 33(5):498–499
Sezonov G, Joseleau-Petit D, D’Ari R (2007) Escherichia coli physiology in Luria–Bertani broth. J Bacteriol 189(23):8746–8749. doi:10.1128/Jb.01368-07
Agnihotri S, Mukherji S, Mukherji S (2014) Size-controlled silver nanoparticles synthesized over the range 5–100 nm using the same protocol and their antibacterial efficacy. RSC Adv 4(8):3974–3983. doi:10.1039/C3ra44507k
Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52(4):662–668. doi:10.1002/1097-4636(20001215)52:4<662:AID-JBM10>3.0.CO;2-3
Rietschel ET, Kirikae T, Schade FU, Mamat U, Schmidt G, Loppnow H, Ulmer AJ, Zahringer U, Seydel U, Di Padova F et al (1994) Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J 8(2):217–225
Park HJ, Kim JY, Kim J, Lee JH, Hahn JS, Gu MB, Yoon J (2009) Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res 43(4):1027–1032. doi:10.1016/j.watres.2008.12.002
Robinson TP, Ocio MJ, Kaloti A, Mackey BM (1998) The effect of the growth environment on the lag phase of Listeria monocytogenes. Int J Food Microbiol 44(1–2):83–92 S0168-1605(98)00120-2
Li WR, Xie XB, Shi QS, Zeng HY, Ou-Yang YS, Chen YB (2010) Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl Microbiol Biotechnol 85(4):1115–1122. doi:10.1007/s00253-009-2159-5
Zeiri L, Bronk BV, Shabtai Y, Eichler J, Efrima S (2004) Surface-enhanced Raman spectroscopy as a tool for probing specific biochemical components in bacteria. Appl Spectrosc 58(1):33–40. doi:10.1366/000370204322729441
Friedrich T (1998) The NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. Biochim Biophys Acta 1364(2):134–146
Cecchini G, Schroder I, Gunsalus RP, Maklashina E (2002) Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta 1553(1–2):140–157
Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37(2):239–253
Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PK, Chiu JF, Che CM (2006) Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 5(4):916–924. doi:10.1021/pr0504079
Letellier L, Shechter E (1979) Cyanine dye as monitor of membrane potentials in Escherichia coli cells and membrane vesicles. Eur J Biochem 102(2):441–447
Sonntag I, Schwarz H, Hirota Y, Henning U (1978) Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J Bacteriol 136(1):280–285
Acknowledgements
This work was supported in part by the National Science Foundation (CHE-1012258, CHE-1265635 and DMR-1409396). TEM work was carried out at the National Center for Electron Microscopy at the Lawrence Berkeley National Laboratory as part of a user project. The PXRD data in this work were recorded on a Rigaku SmartLab instrument supported by the NSF Major Research Instrumentation (MRI) Program under Grant DMR-1126845.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
10853_2015_8847_MOESM1_ESM.pdf
Electronic Supplementary Information. Shape distribution of faceted silver nanostructures, representative high-resolution TEM image of a silver nanoprism, and summary of antimicrobial activity of seed nanoparticles and faceted nanostructures. (PDF 618 kb)
Rights and permissions
About this article
Cite this article
Rojas-Andrade, M., Cho, A.T., Hu, P. et al. Enhanced antimicrobial activity with faceted silver nanostructures. J Mater Sci 50, 2849–2858 (2015). https://doi.org/10.1007/s10853-015-8847-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10853-015-8847-x