A Sustainable Approach for the Green Synthesis of Silver Nanoparticles from Solibacillus isronensis sp. and Their Application in Biofilm Inhibition
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Isolation and 16S rRNA Gene Sequencing
2.3. Extracellular Synthesis of Silver Nanoparticles
2.4. Characterization of Silver Nanoparticles
2.4.1. Nanoparticles Size and Shape Characterizations
2.4.2. Nanoparticles Surface Study by Fourier Transform-Infrared Spectroscopy (FT-IR)
2.4.3. Detection and Quantification of Nanoparticles by Single-Particle Inductively Coupled Plasma-Mass Spectrometry (sp-ICP-MS)
2.4.4. Nanoparticles’ Stability
2.5. Silver Nanoparticles Application in Biofilm Inhibition
2.5.1. Bacterial Strains and Culture Media
2.5.2. Bacteriostatic and Bactericidal Activity
2.5.3. Biofilm Inhibition Assay
2.5.4. Viability of Biofilm Bacteria with Silver Nanoparticle Exposure
2.5.5. Statistical Analysis
3. Results
3.1. Characterization of Strain
3.2. Green Synthesis of Silver Nanoparticles
3.3. Optimization and Kinetics of Conversion of Silver Ions into Nanoparticles
3.4. Characterization of Silver Nanoparticles
3.4.1. Nanoparticles Size and Shape Characterization
3.4.2. Nanoparticles Surface Study
3.4.3. Nanoparticle Stability Study
3.5. Biofilm Inhibition by Silver Nanoparticles
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Dibrov, P.; Dzioba, J.; Gosink, K.K.; Hase, C.C. Chemiosmotic mechanism of antimicrobial activity of Ag(+) in Vibrio cholerae. Antimicrob. Agents Chemother. 2002, 46, 2668–2670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Polivkova, M.; Hubacek, T.; Staszek, M.; Svorcik, V.; Siegel, J. Antimicrobial Treatment of Polymeric Medical Devices by Silver Nanomaterials and Related Technology. Int. J. Mol. Sci. 2017, 18, 419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, H.; Du, J.; Yi, T.H. Green and rapid synthesis of silver nanoparticles using Borago officinalis leaf extract: Anticancer and antibacterial activities. Artif. Cells Nanomed. Biotechnol. 2017, 45, 1310–1316. [Google Scholar] [CrossRef] [Green Version]
- Khatami, M.; Zafarnia, N.; Heydarpoor Bami, M.; Sharifi, I.; Singh, H. Antifungal and antibacterial activity of densely dispersed silver nanospheres with homogeneity size which synthesized using chicory: An in vitro study. J. Mycol. Med. 2018, 28, 637–644. [Google Scholar] [CrossRef]
- Burdusel, A.C.; Gherasim, O.; Grumezescu, A.M.; Mogoanta, L.; Ficai, A.; Andronescu, E. Biomedical Applications of Silver Nanoparticles: An Up-to-Date Overview. Nanomaterials 2018, 8, 681. [Google Scholar] [CrossRef] [Green Version]
- Ullah Khan, S.; Saleh, T.A.; Wahab, A.; Khan, M.H.U.; Khan, D.; Ullah Khan, W.; Rahim, A.; Kamal, S.; Ullah Khan, F.; Fahad, S. Nanosilver: New ageless and versatile biomedical therapeutic scaffold. Int. J. Nanomed. 2018, 13, 733–762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khatami, M.; Mortazavi, S.M.; Kishani-Farahani, Z.; Amini, A.; Amini, E.; Heli, H. Biosynthesis of Silver Nanoparticles Using Pine Pollen and Evaluation of the Antifungal Efficiency. Iran. J. Biotechnol. 2017, 15, 95–101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, H.; Du, J.; Singh, P.; Yi, T.H. Role of green silver nanoparticles synthesized from Symphytum officinale leaf extract in protection against UVB-induced photoaging. J. Nanostruct. Chem. 2018, 8, 359–368. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.J.; Zhang, D.; Yang, D.C. Biological Synthesis of Nanoparticles from Plants and Microorganisms. Trends Biotechnol. 2016, 34, 588–599. [Google Scholar] [CrossRef]
- Singh, P.; Singh, H.; Ahn, S.; Castro-Aceituno, V.; Jimenez, Z.; Simu, S.Y.; Kim, Y.J.; Yang, D.C. Pharmacological importance, characterization and applications of gold and silver nanoparticles synthesized by Panax ginseng fresh leaves. Artif. Cells Nanomed. Biotechnol. 2017, 45, 1415–1424. [Google Scholar] [CrossRef] [Green Version]
- Huh, A.J.; Kwon, Y.J. “Nanoantibiotics”: A new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J. Control. Release Off. J. Control. Release Soc. 2011, 156, 128–145. [Google Scholar] [CrossRef] [PubMed]
- Branda, S.S.; Vik, S.; Friedman, L.; Kolter, R. Biofilms: The matrix revisited. Trends Microbiol. 2005, 13, 20–26. [Google Scholar] [CrossRef] [PubMed]
- Mann, E.E.; Wozniak, D.J. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol. Rev. 2012, 36, 893–916. [Google Scholar] [CrossRef] [Green Version]
- Pandit, S.; Cai, J.N.; Jung, J.E.; Jeon, J.G. Effect of 1-Minute Fluoride Treatment on Potential Virulence and Viability of a Cariogenic Biofilm. Caries Res. 2015, 49, 449–457. [Google Scholar] [CrossRef]
- Nowack, B.; Krug, H.F.; Height, M. 120 years of nanosilver history: Implications for policy makers. Environ. Sci. Technol. 2011, 45, 1177–1183. [Google Scholar] [CrossRef]
- Du, J.; Singh, H.; Yi, T.H. Antibacterial, anti-biofilm and anticancer potentials of green synthesized silver nanoparticles using benzoin gum (Styrax benzoin) extract. Bioprocess. Biosyst. Eng. 2016, 39, 1923–1931. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.J.; Singh, H.; Wang, C.; Hwang, K.H.; Farh Mel, A.; Yang, D.C. Biosynthesis, characterization, and antimicrobial applications of silver nanoparticles. Int. J. Nanomed. 2015, 10, 2567–2577. [Google Scholar]
- Singh, H.; Du, J.; Singh, P.; Yi, T.H. Extracellular synthesis of silver nanoparticles by Pseudomonas sp. THG-LS1.4 and their antimicrobial application. J. Pharm. Anal. 2018, 8, 258–264. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.-J.; Nguyen, N.-L.; Hoang, V.-A.; Sukweenadhi, J.; Farh, M.E.-A.; Yang, D.-C. Cupriavidus yeoncheonense sp. nov., isolated from soil of ginseng. Antonie Van Leeuwenhoek 2015, 107, 749–758. [Google Scholar] [CrossRef]
- Kim, D.H.; Singh, P.; Farh Mel, A.; Kim, Y.J.; Nguyen, N.L.; Lee, H.A.; Yang, D.C. Flavobacterium panacis sp. nov., isolated from rhizosphere of Panax ginseng. Antonie Van Leeuwenhoek 2016, 109, 1199–1208. [Google Scholar] [CrossRef]
- Singh, P.; Singh, H.; Kim, Y.J.; Yang, D.C. Pedobacter panacis sp. nov., isolated from Panax ginseng soil. Antonie Van Leeuwenhoek 2017, 110, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Singh, P.; Kim, Y.J.; Farh Mel, A.; Dan, W.D.; Kang, C.H.; Yang, D.C. Chryseobacterium panacis sp. nov., isolated from ginseng soil. Antonie Van Leeuwenhoek 2016, 109, 187–196. [Google Scholar] [CrossRef] [PubMed]
- Singh, P.; Kim, Y.J.; Singh, H.; Farh, M.E.; Yang, D.C. Achromobacter panacis sp. nov., isolated from rhizosphere of Panax ginseng. J. Microbiol. 2017, 55, 428–434. [Google Scholar] [CrossRef] [PubMed]
- Singh, P.; Singh, H.; Kim, Y.J.; Mathiyalagan, R.; Wang, C.; Yang, D.C. Extracellular synthesis of silver and gold nanoparticles by Sporosarcina koreensis DC4 and their biological applications. Enzym. Microb. Technol. 2016, 86, 75–83. [Google Scholar] [CrossRef]
- Jo, J.H.; Singh, P.; Kim, Y.J.; Wang, C.; Mathiyalagan, R.; Jin, C.G.; Yang, D.C. Pseudomonas deceptionensis DC5-mediated synthesis of extracellular silver nanoparticles. Artif. Cells Nanomed. Biotechnol. 2016, 44, 1576–1581. [Google Scholar] [CrossRef] [Green Version]
- Singh, H.; Du, J.; Singh, P.; Yi, T.H. Ecofriendly synthesis of silver and gold nanoparticles by Euphrasia officinalis leaf extract and its biomedical applications. Artif. Cells Nanomed. Biotechnol. 2018, 46, 1163–1170. [Google Scholar] [CrossRef] [Green Version]
- Kang, J.P.; Kim, Y.J.; Singh, P.; Huo, Y.; Soshnikova, V.; Markus, J.; Ahn, S.; Chokkalingam, M.; Lee, H.A.; Yang, D.C. Biosynthesis of gold and silver chloride nanoparticles mediated by Crataegus pinnatifida fruit extract: In vitro study of anti-inflammatory activities. Artif. Cells Nanomed. Biotechnol. 2017, 1–11. [Google Scholar] [CrossRef]
- Singh, P.; Pandit, S.; Garnaes, J.; Tunjic, S.; Mokkapati, V.R.; Sultan, A.; Thygesen, A.; Mackevica, A.; Mateiu, R.V.; Daugaard, A.E.; et al. Green synthesis of gold and silver nanoparticles from Cannabis sativa (industrial hemp) and their capacity for biofilm inhibition. Int. J. Nanomed. 2018, 13, 3571–3591. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.J.; Wang, C.; Mathiyalagan, R.; Yang, D.C. The development of a green approach for the biosynthesis of silver and gold nanoparticles by using Panax ginseng root extract, and their biological applications. Artif. Cells Nanomed. Biotechnol. 2016, 44, 1150–1157. [Google Scholar] [CrossRef] [Green Version]
- Singh, P.; Kim, Y.J.; Wang, C.; Mathiyalagan, R.; El-Agamy Farh, M.; Yang, D.C. Biogenic silver and gold nanoparticles synthesized using red ginseng root extract, and their applications. Artif. Cells Nanomed. Biotechnol. 2016, 44, 811–816. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.J.; Yang, D.C. A strategic approach for rapid synthesis of gold and silver nanoparticles by Panax ginseng leaves. Artif. Cells Nanomed. Biotechnol. 2016, 44, 1949–1957. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abbai, R.; Mathiyalagan, R.; Markus, J.; Kim, Y.J.; Wang, C.; Singh, P.; Ahn, S.; Farh Mel, A.; Yang, D.C. Green synthesis of multifunctional silver and gold nanoparticles from the oriental herbal adaptogen: Siberian ginseng. Int. J. Nanomed. 2016, 11, 3131–3143. [Google Scholar]
- Pace, H.E.; Rogers, N.J.; Jarolimek, C.; Coleman, V.A.; Higgins, C.P.; Ranville, J.F. Determining transport efficiency for the purpose of counting and sizing nanoparticles via single particle inductively coupled plasma mass spectrometry. Anal. Chem. 2011, 83, 9361–9369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, P.; Ahn, S.; Kang, J.P.; Veronika, S.; Huo, Y.; Singh, H.; Chokkaligam, M.; El-Agamy Farh, M.; Aceituno, V.C.; Kim, Y.J.; et al. In vitro anti-inflammatory activity of spherical silver nanoparticles and monodisperse hexagonal gold nanoparticles by fruit extract of Prunus serrulata: A green synthetic approach. Artif. Cells Nanomed. Biotechnol. 2018, 46, 2022–2032. [Google Scholar]
- Pandit, S.; Chang, K.W.; Jeon, J.G. Effects of Withania somnifera on the growth and virulence properties of Streptococcus mutans and Streptococcus sobrinus at sub-MIC levels. Anaerobe 2013, 19, 1–8. [Google Scholar] [CrossRef]
- Pandit, S.; Kim, J.E.; Jung, K.H.; Chang, K.W.; Jeon, J.G. Effect of sodium fluoride on the virulence factors and composition of Streptococcus mutans biofilms. Arch. Oral Biol. 2011, 56, 643–649. [Google Scholar] [CrossRef]
- Checinska Sielaff, A.; Kumar, R.M.; Pal, D.; Mayilraj, S.; Venkateswaran, K. Solibacillus kalamii sp. nov., isolated from a high-efficiency particulate arrestance filter system used in the International Space Station. Int. J. Syst. Evol. Microbiol. 2017, 67, 896–901. [Google Scholar] [CrossRef]
- Singh, P.; Kim, Y.J.; Singh, H.; Mathiyalagan, R.; Wang, C.; Yang, D.C. Biosynthesis of Anisotropic Silver Nanoparticles by Bhargavaea indica and Their Synergistic Effect with Antibiotics against Pathogenic Microorganisms. J. Nanomater. 2015, 2015, 10. [Google Scholar] [CrossRef] [Green Version]
- Singh, H.; Du, J.; Yi, T.H. Biosynthesis of silver nanoparticles using Aeromonas sp. THG-FG1.2 and its antibacterial activity against pathogenic microbes. Artif. Cells Nanomed. Biotechnol. 2017, 45, 584–590. [Google Scholar] [CrossRef] [Green Version]
- Singh, H.; Du, J.; Yi, T.H. Kinneretia THG-SQI4 mediated biosynthesis of silver nanoparticles and its antimicrobial efficacy. Artif. Cells Nanomed. Biotechnol. 2017, 45, 602–608. [Google Scholar] [CrossRef] [Green Version]
- Singh, P.; Kim, Y.J.; Wang, C.; Mathiyalagan, R.; Yang, D.C. Weissella oryzae DC6-facilitated green synthesis of silver nanoparticles and their antimicrobial potential. Artif. Cells Nanomed. Biotechnol. 2016, 44, 1569–1575. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Taglietti, A.; Diaz Fernandez, Y.A.; Amato, E.; Cucca, L.; Dacarro, G.; Grisoli, P.; Necchi, V.; Pallavicini, P.; Pasotti, L.; Patrini, M. Antibacterial activity of glutathione-coated silver nanoparticles against Gram positive and Gram negative bacteria. Langmuir ACS J. Surf. Colloids 2012, 28, 8140–8148. [Google Scholar] [CrossRef] [PubMed]
- Regiel-Futyra, A.; Kus-Liskiewicz, M.; Sebastian, V.; Irusta, S.; Arruebo, M.; Kyziol, A.; Stochel, G. Development of noncytotoxic silver-chitosan nanocomposites for efficient control of biofilm forming microbes. RSC Adv. 2017, 7, 52398–52413. [Google Scholar] [CrossRef] [Green Version]
- Qing, Y.; Cheng, L.; Li, R.; Liu, G.; Zhang, Y.; Tang, X.; Wang, J.; Liu, H.; Qin, Y. Potential antibacterial mechanism of silver nanoparticles and the optimization of orthopedic implants by advanced modification technologies. Int. J. Nanomed. 2018, 13, 3311–3327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pompilio, A.; Geminiani, C.; Bosco, D.; Rana, R.; Aceto, A.; Bucciarelli, T.; Scotti, L.; Di Bonaventura, G. Electrochemically Synthesized Silver Nanoparticles Are Active Against Planktonic and Biofilm Cells of Pseudomonas aeruginosa and Other Cystic Fibrosis-Associated Bacterial Pathogens. Front. Microbiol. 2018, 9, 1349. [Google Scholar] [CrossRef] [Green Version]
- Roy, A.; Bulut, O.; Some, S.; Mandal, A.K.; Yilmaz, M.D. Green synthesis of silver nanoparticles: Biomolecule-nanoparticle organizations targeting antimicrobial activity. RSC Adv. 2019, 9, 2673–2702. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.; Mathiyalagan, R.; Kim, Y.J.; Castro-Aceituno, V.; Singh, P.; Ahn, S.; Wang, D.; Yang, D.C. Rapid green synthesis of silver and gold nanoparticles using Dendropanax morbifera leaf extract and their anticancer activities. Int. J. Nanomed. 2016, 11, 3691–3701. [Google Scholar]
- Oh, K.H.; Soshnikova, V.; Markus, J.; Kim, Y.J.; Lee, S.C.; Singh, P.; Castro-Aceituno, V.; Ahn, S.; Kim, D.H.; Shim, Y.J.; et al. Biosynthesized gold and silver nanoparticles by aqueous fruit extract of Chaenomeles sinensis and screening of their biomedical activities. Artif. Cells Nanomed. Biotechnol. 2018, 46, 599–606. [Google Scholar] [CrossRef] [Green Version]
- Schrofel, A.; Kratosova, G.; Safarik, I.; Safarikova, M.; Raska, I.; Shor, L.M. Applications of biosynthesized metallic nanoparticles—A review. Acta Biomater. 2014, 10, 4023–4042. [Google Scholar] [CrossRef]
- Peulen, T.O.; Wilkinson, K.J. Diffusion of nanoparticles in a biofilm. Environ. Sci. Technol. 2011, 45, 3367–3373. [Google Scholar] [CrossRef]
- Loo, C.Y.; Young, P.M.; Cavaliere, R.; Whitchurch, C.B.; Lee, W.H.; Rohanizadeh, R. Silver nanoparticles enhance Pseudomonas aeruginosa PAO1 biofilm detachment. Drug Dev. Ind. Pharm. 2014, 40, 719–729. [Google Scholar] [CrossRef] [PubMed]
- Ikuma, K.; Decho, A.W.; Lau, B.L. When nanoparticles meet biofilms-interactions guiding the environmental fate and accumulation of nanoparticles. Front. Microbiol. 2015, 6, 591. [Google Scholar] [CrossRef] [PubMed]
- Kittler, S.; Greulich, C.; Diendorf, J.; Köller, M.; Epple, M. Toxicity of Silver Nanoparticles Increases during Storage Because of Slow Dissolution under Release of Silver Ions. Chem. Mater. 2010, 22, 4548–4554. [Google Scholar] [CrossRef]
Sample Availability: Samples of the compounds are not available from the authors. |
Type of Bond | Cells Wavenumber (cm−1) | AgNPs Wavenumber (cm−1) |
---|---|---|
O-H strech | 3279.90 | - |
C-H strech | 2928.48 | 2868.39 |
Alkyne group | 2165.49, 2050.31, 1098.17 | 2323.13, 2084.22, 1980.93 |
C=C strech, amide C=O strech | 1634.18, 1532.00 | 1732.42,1651.76,1567.94–1505.54 |
CH3, CH2 asymmetric deformation | 1454.69, 1392.99 | 1429.02 |
C-O strech | 1058.90 | 980.84 |
C-C deformation | - | 684.26, 563.81 |
Strains | MIC (µg/mL) | MBC (µg/mL) |
---|---|---|
E. coli | 3.12 | 6.25 |
P. aeruginosa | 1.56 | 3.12 |
S. epidermidis | 25 | 50 |
S. aureus | 50 | 50 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Singh, P.; Pandit, S.; Mokkapati, V.; Garnæs, J.; Mijakovic, I. A Sustainable Approach for the Green Synthesis of Silver Nanoparticles from Solibacillus isronensis sp. and Their Application in Biofilm Inhibition. Molecules 2020, 25, 2783. https://doi.org/10.3390/molecules25122783
Singh P, Pandit S, Mokkapati V, Garnæs J, Mijakovic I. A Sustainable Approach for the Green Synthesis of Silver Nanoparticles from Solibacillus isronensis sp. and Their Application in Biofilm Inhibition. Molecules. 2020; 25(12):2783. https://doi.org/10.3390/molecules25122783
Chicago/Turabian StyleSingh, Priyanka, Santosh Pandit, VRSS Mokkapati, Jørgen Garnæs, and Ivan Mijakovic. 2020. "A Sustainable Approach for the Green Synthesis of Silver Nanoparticles from Solibacillus isronensis sp. and Their Application in Biofilm Inhibition" Molecules 25, no. 12: 2783. https://doi.org/10.3390/molecules25122783