Biosynthesis of gold nanoparticles by the extreme bacterium Deinococcus radiodurans and an evaluation of their antibacterial properties

Abstract

Deinococcus radiodurans is an extreme bacterium known for its high resistance to stresses including radiation and oxidants. The ability of D. radiodurans to reduce Au(III) and biosynthesize gold nanoparticles (AuNPs) was investigated in aqueous solution by ultraviolet and visible (UV/Vis) absorption spectroscopy, electron microscopy, X-ray diffraction (XRD), dynamic light scattering (DLS), Fourier transform infrared spectroscopy (FTIR) and X-ray photoelectron spectroscopy (XPS). D. radiodurans efficiently synthesized AuNPs from 1 mM Au(III) solution in 8 h. The AuNPs were of spherical, triangular and irregular shapes with an average size of 43.75 nm and a polydispersity index of 0.23 as measured by DLS. AuNPs were distributed in the cell envelope, across the cytosol and in the extracellular space. XRD analysis confirmed the crystallite nature of the AuNPs from the cell supernatant. Data from the FTIR and XPS showed that upon binding to proteins or compounds through interactions with carboxyl, amine, phospho and hydroxyl groups, Au(III) may be reduced to Au(I), and further reduced to Au(0) with the capping groups to stabilize the AuNPs. Biosynthesis of AuNPs was optimized with respect to the initial concentration of gold salt, bacterial growth period, solution pH and temperature. The purified AuNPs exhibited significant antibacterial activity against both Gram-negative (Escherichia coli) and Gram-positive (Staphylococcus aureus) bacteria by damaging their cytoplasmic membrane. Therefore, the extreme bacterium D. radiodurans can be used as a novel bacterial candidate for efficient biosynthesis of AuNPs, which exhibited potential in biomedical application as an antibacterial agent.

Keywords:

• Deinococcus radiodurans
• gold nanoparticles
• gold ions
• reduction
• antibacterial

Supplementary materials

Figure S1 Formation of AuNPs by Deinococcus radiodurans cell pellets in the presence of Au(III).

Notes: (A) The absorbance spectra of D. radiodurans cells (DR) in the presence of 1 mM Au(III) and the control (CK, D. radiodurans cells in the absence of Au(III)). (B) The color of D. radiodurans pellets with (1) or (2) without 1 mM Au(III). (C) The prepared AuNPs from the supernatant of D. radiodurans cells in the presence of Au(III). Left, supernatant; right, purified AuNPs powder obtained by dialysis and lyophilization of the supernatant.

Abbreviation: AuNPs, gold nanoparticles.

Figure S2 XPS spectrum of the core level of C_1s in the purified AuNPs.

Notes: The C_1s spectrum could be resolved into four components that can bind to nanoparticle surface, consistent with previous reports.^10,11 The peak at binding energies at 284.6 eV corresponded to C–C and C–H. Carbon bonded with nitrogen (C–N) and hydroxyl groups (C–OH) had binding energies at 285.6 and 286.7 eV, respectively. The peak at 287.8 eV was attributed to carbonyl groups.

Abbreviations: XPS, X-ray photoelectron spectroscopy; AuNPs, gold nanoparticles.

Table S1 List of bacteria that synthesize gold nanoparticles

References

• DuLJiangHLiuXWangEBiosynthesis of gold nanoparticles assisted by Escherichia coli DH5α and its application on direct electrochemistry of hemoglobinElectrochem Commun20079511651170
   Web of Science ®Google Scholar
• Correa-LlanténDNMuñoz-IbacacheSACastroMEMuñozPABlameyJMGold nanoparticles synthesized by Geobacillus sp. strain ID17 a thermophilic bacterium isolated from Deception Island, AntarcticaMicrob Cell Fact2013127523919572
   PubMed Web of Science ®Google Scholar
• HeSGuoZZhangYBiosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulataMater Lett2007611839843987
   Web of Science ®Google Scholar
• SrivastavaSKYamadaROginoCKondoABiogenic synthesis and characterization of gold nanoparticles by Escherichia coli K12 and its heterogeneous catalysis in degradation of 4-nitrophenolNanoscale Res Lett2013817023399317
   PubMedGoogle Scholar
• SureshAKPelletierDAWangWBiofabrication of discrete spherical gold nanoparticles using the metal-reducing bacterium Shewanella oneidensisActa Biomater2011752148215221241833
   PubMed Web of Science ®Google Scholar
• KalishwaralalKDeepakVRam Kumar PandianSBiosynthesis of silver and gold nanoparticles using Brevibacterium caseiColloids Surf B Biointerfaces201077225726220197229
   PubMed Web of Science ®Google Scholar
• ReithFEtschmannBGrosseCMechanisms of gold biomineralization in the bacterium Cupriavidus metalliduransProc Natl Acad Sci U S A200910642177571776219815503
   PubMed Web of Science ®Google Scholar
• HusseinyMIEl-AzizMABadrYMahmoudMABiosynthesis of gold nanoparticles using Pseudomonas aeruginosaSpectrochim Acta A Mol Biomol Spectrosc2007673–41003100617084659
   PubMed Web of Science ®Google Scholar
• JenaSDasBBosuRSuarMMandalDBacteria generated antibacterial gold nanoparticles and potential mechanistic insightJ Cluster Sci2015265115
   Web of Science ®Google Scholar
• DasSKDickinsonCLafirFBroughamDFMarsiliESynthesis, characterization and catalytic activity of gold nanoparticles biosynthesized with Rhizopus oryzae protein extractGreen Chem201214513221334
   Web of Science ®Google Scholar
• DasSKLiangJSchmidtMLaffirFMarsiliEBiomineralization mechanism of gold by zygomycete fungi Rhizopous oryzaeACS Nano2012676165617322708541
   PubMed Web of Science ®Google Scholar

Acknowledgments

The authors thank Dr Yangfan Lu at the School of Materials Science and Engineering of Zhejiang University for the help in XPS analysis. This work was supported by grants from the National Natural Science Foundation of China (31370119, 31170079, 31210103904, 31370102), a major project for genetically modified organisms breeding from the Ministry of Agriculture of China (2013ZX08009003-002) and the Natural Science Foundation of Zhejiang Province (LY13C010001).

Disclosure

The authors report no conflicts of interest in this work.