Skip to main content

Advertisement

SpringerLink
Log in

Unnatural amino acid-mediated synthesis of silver nanoparticles and their antifungal activity against Candida species

  • Research Paper
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

In this study, the biocompatible unnatural amino acid, 3,4-dihydroxy-l-phenylalanine (l-dopa), which is used in protein engineering, was employed in the facile synthesis of silver nanoparticles (AgNPs). The surface plasmon resonance (SPR) band of the UV–Vis spectrum at 406 nm demonstrates the possibility of formation of smaller nanoparticles; the symmetrical shape of the band demonstrates a narrow size distribution of AgNPs, the formation of AgNPs, and the face-centered cubic (fcc) crystalline structure of nanoparticles was confirmed by X-ray diffraction (XRD). Additionally, transmission electron microscopic (TEM) images revealed that these particles were spherical in shape with diameters of 2.7–12.2 nm (average = 8.7 nm). These nanoparticles exhibited antifungal activity against both planktonic and biofilm yeast cells of Candida albicans and C. dubliniensis. The minimum inhibitory concentrations (MICs) and minimum fungicidal concentrations (MFCs) were determined by microdilution assays. C. albicans were shown to be less susceptible than C. dubliniensis to AgNPs based on the MIC (ranging from 7.8 to 15.6 µg ml−1) and MFC (ranging from 31.2 to 62.5 µg ml−1). With regard to biomass quantification, AgNPs did not induce a significant reduction of the biomass of Candida species; however, treatment of biofilm with 500 µg/ml of AgNPs induced a 2.99−log10 (P < 0.001) and 3.53−log10 (P < 0.001) significant reduction in the number of culturable cells of CFUs when compared to control samples of C. albicans and C. dubliniensis, respectively. Thus, AgNPs-based antifungal agents would be an effective alternative to conventional drugs to overcome drug resistance in Candida-associated infections.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alfonta L, Zhang Z, Uryu S, Loo JA, Schultz PG (2003) Site-specific incorporation of a redox-active amino acid into proteins. J Am Chem Soc 125:14662–14663

    Article  Google Scholar 

  • Alivisatos AP (1996) Perspectives on the physical chemistry of semiconductor nanocrystals. J Phys Chem 100:13226–13239

    Google Scholar 

  • AshaRani PV, Mun GLK, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290

    Article  Google Scholar 

  • Balazs DJ, Triandafillu K, Wood P, Chevolot Y, van Delden C, Harms H, Hollenstein C, Mathieu HJ (2004) Inhibition of bacterial adhesion on PVC endotracheal tubes by RF-oxygen glow discharge, sodium hydroxide and silver nitrate treatments. Biomaterials 25:2139–2151

    Article  Google Scholar 

  • Coco BJ, Bagg J, Cross LJ, Jose A, Cross J, Ramage G (2008) Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol Immunol 23:377–383

    Article  Google Scholar 

  • d’Enfert C, Hube B (eds) (2007) Candida: comparative and functional genomics. Caister Academic Press, Norfolk

    Google Scholar 

  • Di Marco M, Shamsuddin S, Razak KA, Aziz AA, Devaux C, Borghi E, Levy L, Sadun C (2010) Overview of the main methods used to combine proteins with nanosystems: absorption, bioconjugation, and encapsulation. Int J Nanomed 5:37–49

    Google Scholar 

  • Durmus NG, Webster TJ (2013) Eradicating antibiotic-resistant biofilms with silver-conjugated superparamagnetic iron oxide nanoparticles. Adv Health C Mater 2:165–171

    Article  Google Scholar 

  • Jaber M, Bouchoucha M, Delmotte L, Methivier C, Lambert JF (2011) Fate of l-dopa in the presence of inorganic matrices: vectorization or composite material formation? J Phys Chem C 115:19216–19225

    Article  Google Scholar 

  • Jin Y, Samaranayake LP, Samaranayake Y, Yip HK (2004) Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch Oral Biol 49:789–798

    Article  Google Scholar 

  • Kalathil S, Lee J, Cho MH (2011) Electrochemically active biofilm-mediated synthesis of silver nanoparticles in water. Green Chem 13:1482–1485

    Article  Google Scholar 

  • Kalishwaralal K, BarathManiKanth S, Pandian S, Deepak V, Gurunathan S (2010) Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococus epidermidis. Colloids Surf B Biointerface 79:340–344

    Article  Google Scholar 

  • Kumbhar AS, Padhye SB, Saraf AP, Mahajan HB, Chopade BA, West DX (1991) Novel broad-spectrum metal-based antifungal agents. Correlations amongst the structural and biological properties of copper(II)2-acetylpyridine N4-dialkylthiosemicarbazones. Biol Met 4:141–143

    Article  Google Scholar 

  • Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007

    Article  Google Scholar 

  • Li X, Wang L, Fan Y, Feng Q, Cui F (2012) Biocompatibility and toxicity of nanoparticles and nanotubes. J Nanomater 2012:548389

    Google Scholar 

  • Liao Y, Wang Y, Feng X, Wang W, Xu F, Zhang L (2010) Antibacterial surfaces through dopamine functionalization and silver nanoparticle immobilization. Mater Chem Phys 121:534–540

    Google Scholar 

  • Lipovsky A, Nitzan Y, Gedanken A, Lubart R (2011) Antifungal activity of ZnO nanoparticles—the role of ROS mediated cell injury. Nanotechnology 22:105101

    Article  Google Scholar 

  • Liu Z, Niu H, Wu S, Huang R (2014) CsgD regulatory network in a bacterial trait-altering biofilm formation. Emerg Microbes Infect 3:e1

    Article  Google Scholar 

  • Ma Z, Han H (2008) One-step synthesis of cystine-coated gold nanoparticles in aqueous solution. Colloids Surf A Physicochem Eng Asp 317:229–233

    Article  Google Scholar 

  • Maity I, Manna MK, Rasale DB, Das AK (2014) Peptide-nanofiber-supported palladium nanoparticles as an efficient catalyst for the removal of N-terminus protecting groups. ChemPlusChem 79:413–420

    Article  Google Scholar 

  • Mandal S, Selvakannan PR, Phadtare S, Pasricha R, Sastry M (2002) Synthesis of a stable gold hydrosol by the reduction of chloroaurate ions by the amino acid, aspartic acid. Proc Indian Acad Sci (Chem Sci) 114:513–520

    Google Scholar 

  • Margiotta N, Bergamo A, Sava G, Padovano G, de Clercq E, Natile G (2004) Antiviral properties and cytotoxic activity of platinum(II) complexes with 1,10-phenanthrolines and acyclovir or penciclovir. J Inorg Biochem 98:1385–1390

    Article  Google Scholar 

  • Mazzola PG, Jozala AF, Novaes LCL, Moriel P, Christina T, Penna V (2009) Minimal inhibitory concentration (MIC) determination of disinfectant and/or sterilizing agents. Braz J Pharm Sci 45:241–248

    Article  Google Scholar 

  • McCann M, Geraghty M, Devereux M, O’Shea D, Mason J, O’Sullivan L (2000) Insights into the mode of action of the anti-Candida activity of 1,10-phenanthroline and its metal chelates. Metal Based Drugs 7:185–193

    Article  Google Scholar 

  • Monteiro DR, Gorup LF, Silva S, Negri M, de Camargo ER, Oliveira R, Barbosa DB, Henriques M (2011) Silver colloidal nanoparticles: antifungal effect against adhered cells and biofilms of Candida albicans and Candida glabrata. Biofouling J Bioadh Biofilm Res 27:711–719

    Article  Google Scholar 

  • Monteiro DR, Silva S, Negri M, Gorup LF, de Camargo ER, Oliveira R, Barbosa DB, Henriques M (2012) Silver nanoparticles: influence of stabilizing agent and diameter on antifungal activity against Candida albicans and Candida glabrata biofilms. Lett Appl Microbiol 54:383–391

    Article  Google Scholar 

  • Narayanan KB, Sakthivel N (2011) Green synthesis of biogenic metal nanoparticles by terrestrial and aquatic phototrophic and heterotrophic eukaryotes and biocompatible agents. Adv Coll Interface Sci 169:59–79

    Article  Google Scholar 

  • Narayanan KB, Sakthivel N (2013) Mycocrystallization of gold ions by the fungus Cylindrocladium floridanum. World J Microbiol Biotechnol 29:2207–2211

    Article  Google Scholar 

  • NCCLS (2002) National committee for Clinical Laboratory Standards, reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard., Document M27-A, NCCLS, Pennsylvania 19087(17):1–29

  • O’Connor L, Caplice N, Coleman DC, Sullivan DJ, Moran GP (2010) Differential filamentation of Candida albicans and Candida dubliniensis is governed by nutrient regulation of UME6 expression. Eukaryot Cell 9:1383–1397

    Article  Google Scholar 

  • Shin JH, Kee SJ, Shin MG, Kim SH, Shin DH, Lee SK, Suh SP, Ryang DW (2002) Biofilm production by isolates of Candida species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol 40:1244–1248

    Article  Google Scholar 

  • Silva S, Henriques M, Oliveira R, Williams D, Azeredo J (2010) In vitro biofilm activity of non-Candida albicans Candida species. Curr Microbiol 61:534–540

    Article  Google Scholar 

  • Sobel JD (1988) Pathogenesis and epidemiology of vulvovaginal candidiasis. Ann NY Acad Sci 544:547–557

    Article  Google Scholar 

  • Stobie N, Duffy B, McCormack DE, Colreavy J, Hidalgo M, McHale P, Hinder SJ (2008) Prevention of Staphylococcus epidermidis biofilm formation using a low-temperature processed silver-doped phenyltriethoxysilane sol–gel coating. Biomaterials 29:963–969

    Article  Google Scholar 

  • Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC (1995) Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141:1507–1521

    Article  Google Scholar 

  • Umeda A, Thibodeaux GN, Zhu J, Lee Y, Jonathan Z (2009) Site-specific protein cross-linking with genetically incorporated 3,4-dihydroxy-l-phenylalanine. ChemBioChem 10:1302–1304

    Article  Google Scholar 

  • Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Kohler JR, Kadosh D, Lopez-Ribot JL (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6(3):e1000828

    Article  Google Scholar 

  • Watamoto T, Samaranayake LP, Jayatilake JA, Egusa H, Yatani H, Seneviratne CJ (2009) Effect of filamentation and mode of growth on antifungal susceptibility of Candida albicans. Int J Antimicrob Agents 34:333–339

    Article  Google Scholar 

  • Watanabe T, Takano M, Ogasawara A, Mikami T, Kobayashi T, Watabe M, Matsumoto T (2000) Anti-Candida activity of a new Platinum derivative. Antimicrob Agents Chemother 44:2853–2854

    Article  Google Scholar 

  • Young JK, Lewinski NA, Langsner RJ, Kennedy LC, Satyanarayan A, Nammalvar V, Lin AY, Drezek RA (2011) Size-controlled synthesis of monodispersed gold nanoparticles via carbon monoxide gas reduction. Nanoscale Res Lett 6:428

    Article  Google Scholar 

  • Zare B, Sepehrizadeh Z, Faramarzi MA, Soltany-Reezaee-Rad M, Rezaie S, Shahverdi AR (2013) Antifungal activity of biogenic tellurium nanoparticles against Candida albicans and its effects on squalene monooxygenase gene expression. Biotechnol Appl Biochem. doi:10.1002/bab.1180

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) of the Ministry of Education, Science and Technology (2013-009083).

Author information

Authors and Affiliations

  1. School of Biotechnology and Graduate School of Biochemistry, Yeungnam University, Gyeongsan, 712–749, South Korea

    Kannan Badri Narayanan & Hyun Ho Park

Authors
  1. Kannan Badri Narayanan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyun Ho Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hyun Ho Park.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Narayanan, K.B., Park, H.H. Unnatural amino acid-mediated synthesis of silver nanoparticles and their antifungal activity against Candida species. J Nanopart Res 16, 2523 (2014). https://doi.org/10.1007/s11051-014-2523-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-014-2523-y

Keywords

Search

Navigation