Abstract
Chemical reagents that are used for synthesis of nanoparticles are often toxic, while biological reagents are safer and cost-effective. Here, the behavior of Staphylococcus epidermidis (ATCC 12228) was evaluated for biosynthesis of silver nanoparticles (Ag-NPs) and cadmium sulfide nanoparticles (CdS-NPs) using TEM images intra- and extracellularly. The bacteria only biosynthesized the nanoparticles intracellularly and distributed Ag-NPs throughout the cytoplasm and on outside surface of cell walls, while CdS-NPs only formed in cytoplasm near the cell wall. A new method for purification of the nanoparticles was used. TEM images of pure CdS-NPs confirmed biosynthesis of agglomerated nanoparticles. Biosynthetic Ag-NPs were more stable against bright light and aggregation reaction than synthetic Ag-NPs (prepared chemically) also biosynthetic Ag-NPs displayed lower toxicity in in vitro assays. CdS-NPs indicated no toxicity in in vitro assays. Biosynthetic nanoparticles as product of the detoxification pathway may be safer and more stable for biosensors.
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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. Colloids Surf B Biointerfaces 28(4):313–318
Anil Kumar S, Abyaneh MK, Gosavi SW, Kulkarni SK, Pasricha R, Ahmad A, Khan MI (2007) Nitrate reductase-mediated synthesis of silver nanoparticles from AgNO3. Biotechnol Lett 29:439–445
Ataei ML, Ebrahimzadeh Bideskan AR (2014) The effects of nano-silver and garlic administration during pregnancy on neuron apoptosis in rat offspring hippocampus. Iran J Basic Med Sci 17(6):411–418
Atashbeyk DG, Khameneh B, Tafaghodi M, Fazly Bazzaz BS (2014) Eradication of methicillin-resistant Staphylococcus aureus infection by nanoliposomes loaded with gentamicin and oleic acid. Pharm Biol 52:1423–1428
Bagheri Abassi F, Alavi H, Mohammadipour A, Motejaded F (2015) The effect of silver nanoparticles on apoptosis and dark neuron production in rat hippocampus. Iran J Basic Med Sci 18(7):644–648
Banyay M, Sarkar M, Graslund A (2003) A library of IR bands of nucleic acids in solution. Biophys Chem 104(2):477–488
Barth A (2007) Infrared spectroscopy of proteins. Biochim Biophys Acta 1767(9):1073–1101
Birla SS, Tiwari VV, Gade AK, Ingle AP, Yadav AP, Rai MK (2009) Fabrication of silver nanoparticles by Phoma glomerata and its combined effect against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Lett Appl Microbiol 48(2):173–179
Bryant KA (2008) Investigation of the Staphylococcus epidermidis macromolecular synthesis operon. University of Nebraska Medical Center, Omaha, p 151
Casal HL, Mantsch HH (1984) Polymorphic phase behavior of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta 779(4):381–401
Chan WCW, Maxwell DJ, Gao XH, Bailey RE, Han MY, Nie SM (2002) Luminescent quantum dots for multiplexed biological detection and imaging. Curr Opin Biotechnol 13:40–46
Cunningham DP, Lundie LL Jr (1993) Precipitation of cadmium by Clostridium thermoaceticum. Appl Environ Microbiol 59(1):7–14
Dahl JA, Maddux BLS, Hutchison JE (2007) Toward greener nanosynthesis. Chem Rev 107:2228–2269
Deepak V, Kalishwaralal K, Kumar Pandian SR, Gurunathan S (2011) An insight into the bacterial biogenesis of silver nanoparticles, industrial production and scale-up. In: Rai M, Duran N (eds) Metal nanoparticles in microbiology. Springer, New York, p 17
Doty RS, Tshikhudo TR, Brust M, Fernig DG (2005) Extremely stable water-soluble Ag nanoparticles. Chem Mater 17(18):4630–4635
Duran N, Marcato PD, Alves OL, DeSouza G, Esposito E (2005) Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. J Nanobiotechnol 3:1–8
El-Shanshoury AR, ElSilk SE, Ebeid ME (2011) Extracellular biosynthesis of silver nanoparticles using Escherichia coli ATCC 8739, Bacillus subtilis ATCC 6633, and Streptococcus thermophilus ESh1 and their antimicrobial activities. ISRN Nanotechnol 2011:1–7
Entenman C (1957) General procedures for separating lipid components of tissue. Method Enzymol 3:299–317
Gadd GM, Griffiths AJ (1978) Microorganisms and heavy metal toxicity. Microb Ecol 4(4):303–317
Gade AK, Bonde P, Ingle AP, Marcato PD, Duran N, Rai MK (2008) Exploitation of Aspergillus niger for synthesis of silver nanoparticles. J Biobased Mater Bioenergy 2:243–247
Gaurav K, Karthik L, Rao KV (2012) Novel microbial route to synthesize ZnO nanoparticles using Aeromonas hydrophila and their activity against pathogenic bacteria and fungi. Spectrochim Acta Part A 90:78–84
Glomm RW (2005) Functionalized gold nanoparticles for applications in bionanotechnology. J Dispers Sci Technol 26:389–414
Hanauer M, Pierrat S, Zins I, Lotz A, Sönnichsen C (2007) Separation of nanoparticles by gel electrophoresis according to size and shape. Nano Lett 7(9):2881–2885
He S, Guo Z, Zhang Y, Zhang S, Wang J, Gu N (2007) Biosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulata. Mater Lett 61:3984–3987
Henglein A (1989) Small-particle research: Physicochemical properties of extremely small colloidal metal and semiconductor particles. Chem Rev 89:1861–1873
Huang T, Nancy-Xu XH (2010) Synthesis and characterization of tunable rainbow colored colloidal silver nanoparticles using single-nanoparticle plasmonic microscopy and spectroscopy. J Mater Chem 20:9867–9876
Ingle A, Gade A, Pierrat S, Sonnichsen C, Rai MK (2008) Mycosynthesis of silver nanoparticles using the fungus Fusarium acuminatum and its activity against some human pathogenic bacteria. Curr Nanosci 4:141–144
Jain V, Jain P (2011) Biomolecules–nanoparticles: interaction in nanoscale. In: Rai M, Duran N (eds) Metal nanoparticles in microbiology. Springer, New York, p 135
Jaiswal JK, Mattoussi H, Mauro JM, Simon SM (2003) Long-termmultiple color imaging of live cells using quantum dot bioconjugates. Nat Biotechnol 21:47–51
Jayaseelan C, Abdul Rahuman A, Kirthi AV, Marimuthu S, Santhoshkumar T, Bagavan A, Kacurakova M, Mathlouthi M (1996) FTIR and laser-Raman spectra of oligosaccharides in water: characterization of the glycosidic bond. Carbohydr Res 284(2):145–157
Konishi Y, Ohno K, Saitoh N, Nomura T, Nagamine S, Hishida H, Takahashi Y (2007a) Bioreductive deposition of platinum nanoparticles on the bacterium Shewanella algae. J Biotechnol 128:648–653
Konishi Y, Tsukiyama T, Tachimi T, Saitoh N, Nomura T, Nagamine S (2007b) Microbial deposition of gold nanoparticles by the metal-reducing bacterium Shewanella algae. Electrochim Acta 53:186–192
Kowshik M, Ashataputre S, Kharrazi S, Kulkarni SK, Paknikari KM, Vogel W, Urban J (2003) Extracellular synthesis of silver nanoparticles by a silver-tolerant yeast strain MKY3. Nanotechnology 14:95–100
Lee KJ, Jun BH, Choi J, Lee YI, Joung J, Oh YS (2007) Environmentally friendly synthesis of organic soluble silver nanoparticles for printed electronics. Nanotechnology 18(33):335601–335605
Lengke MF, Southam G (2005) The effect of thiosulfate-oxidizing bacteria on the stability of the gold-thiosulfate complex. Geochim Cosmochim Acta 69(15):3759–3772
Lengke MF, Southam G (2006) Bioaccumulation of gold by sulfate-reducing bacteria cultured in the presence of gold(I)-thiosulfate complex. Geochim Cosmochim Acta 70:3646–3661
Lengke MF, Fleet ME, Southam G (2006) Morphology of gold nanoparticles synthesized by filamentous cyanobacteria from gold(I)-thiosulfate and gold(III)-chloride complexes. Langmuir 22(6):2780–2787
Lengke MF, Sanpawanitchakit C, Southam G (2011) Biosynthesis of gold nanoparticles: a review. In: Rai M, Duran N (eds) Metal nanoparticles in microbiology. Springer, New York, p 37
Levinson W (2010) Review of medical microbiology and immunology, 11th edn. McGraw-Hill, New York, p 94
Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR, Khan MI, Ramani R, Parischa R, Ajayakumar PV, Alam M, Sastry M, Kumar R (2001) Bioreduction of AuCl4 ions by the fungus, Verticillium sp. and surface trapping of the gold nanoparticles formed. Angew Chem Int Ed 40(19):3585–3588
Mukherjee P, Roy M, Mandal BP, Dey GK, Mukherjee PK, Ghatak J, Tyagi AK, Kale SP (2008) Green synthesis of highly stabilized nanocrystalline silver particles by a non-pathogenic and agriculturally important fungus T. asperellum. Nanotechnology 19:075103
Murray CB, Kagan CR, Bawendi MG (2000) Synthesis and characterization of monodisperse nanocrystals and close packed nanocrystal assemblies. Annu Rev Mater Sci 30:545–610
Nag A, Sapra S, Sengupta S, Prakash A, Ghangrekar A, Periasamy ND, Sarma D (2008) Luminescence in Mn-doped CdS nanocrystals. Bull Mater Sci 31:561–568
Nair B, Pradeep T (2002) Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus strains. Cryst Growth Des 2(4):293–298
Nam JM, Thaxton CS, Mirkin CA, Nam JM, Thaxton CS, Mirkin CA (2003) Nanoparticle-based bio-bar codes for the ultrasensitive detection of proteins. Science 301(5641):1884–1886
Oelshlegel FJ, Schroeder JR, Stahmann MA (1970) A simple procedure for basic hydrolysis of proteins and rapid determination of tryptophan using a starch column. Anal Biochem 34(2):331–337
Paramelle D, Sadovoy A, Gorelik S, Free P, Hobley J, Fernig DG (2014) A rapid method to estimate the concentration of citrate capped silver nanoparticles from UV–visible light spectrum. Analyst 139(19):4855–4861
Pecora R (1985) Dynamic light scattering: applications of photon correlation spectroscopy. Plenum Press, New York, p 35
Rai M, Yadav A, Gade A (2008) Current trends in phytosynthesis of metal nanoparticles. Crit Rev Biotechnol 28(4):277–284
Sabyasachi P, Ashok KP, Debasis S, Ramagiri SV, Bellare JR, Mazumder S (2014) Redox decomposition of silver citrate complex in nanoscale confinement: an unusual mechanism of formation and growth of silver nanoparticles. Langmuir 30(9):2460–2469
Sastry M, Mayya KS, Bandyopadhyay K (1997) pH dependent changes in the optical properties of carboxylic acid reprivatized silver colloidal particles. Colloids Surf A 127:221–228
Schmid G (1992) Large clusters and colloids: metals in the embryonic state. Chem Rev 92:1709–1727
Schultz S, Smith DR, Mock JJ, Schultz DA (2000) Single-target molecule detection with nonbleaching multicolor optical immunolabels. Proc Natl Acad Sci USA 97:996–1001
Sondi I, Salopek Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275(1):177–182
Southam G, Beveridge TJ (1994) The in vitro formation of placer gold by bacteria. Geochim Cosmochim Acta 58(20):4527–4530
Williams P, Keshavarz-Moore E, Dunnill P (1996) Production of cadmium sulphide microcrystallites in batch cultivation by Schizosaccharomyces pombe. J Biotechnol 48:259–267
Wong PT, Wong RK, Caputo TA, Godwin TA, Rigas B (1991) Infrared spectroscopy of exfoliated human cervical cells: evidence of extensive structural changes during carcinogenesis. Proc Natl Acad Sci USA 88(24):10988–10992
Yang C, Zhou X, Wang L, Tian X, Wang Y, Pi Z (2009) Preparation and tunable photoluminescence of alloyed CdSxSe1-x nanorods. J Mater Sci 44:3015–3019
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This research was supported financially (No. 931498) by the Biotechnology Research Center, School of Pharmacy, Mashhad University of Medical Sciences (MUMS), Mashhad, Iran.
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Rezvani Amin, Z., Khashyarmanesh, Z. & Fazly Bazzaz, B.S. Different behavior of Staphylococcus epidermidis in intracellular biosynthesis of silver and cadmium sulfide nanoparticles: more stability and lower toxicity of extracted nanoparticles. World J Microbiol Biotechnol 32, 140 (2016). https://doi.org/10.1007/s11274-016-2110-8
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DOI: https://doi.org/10.1007/s11274-016-2110-8