Green-fabrication of gold nanomaterials using Staphylococcus warneri from Sundarbans estuary: an effective recyclable nanocatalyst for degrading nitro aromatic pollutants

Abstract

Microbial synthesis of gold nanoparticles (GNPs) has attracted considerable attention in recent times due to their exceptional capability for the bioremediation of industrial wastes and also for the treatment of wastewater. A bacterial strain Staphylococcus warneri, isolated from the estuarine mangroves of Sundarbans region produced highly stable GNPs by reducing hydrogen auric chloride (HAucl4) salt using intracellular protein extract. The nanoparticles were characterized utilizing ultraviolet-visible spectrophotometry, transmission electron microscopy, scanning electron microscopy, atomic force microscopy, X-ray diffraction, and surface enhanced Raman scattering. Highly dispersed, spherically shaped GNPs varied around 15–25 nm in size and were highly crystalline with face-centered cubic structures. Recyclable catalytic activity of as-synthesized GNPs was evidenced by complete degradation of nitro aromatic pollutants like 2-nitroaniline, 4-nitroaniline, 2-nitrophenol and 4-nitrophenol. Our GNPs show excellent and efficient catalytic activity with significantly high rate constant (10−1 order) and high turnover frequency (103 order) in recyclable manner up to three times. To our knowledge, this is the first report of Staphylococcus warneri in the production of gold nanoparticles. This green technology for bioremediation of toxic nitro aromatic pollutants is safe and economically beneficial to challenge the development and sustainability issue.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  1. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    CAS  Article  Google Scholar 

  2. Anantharaj S, Jayachandran M, Kundu S (2016) Unprotected and interconnected Ru 0 nano-chain networks: advantages of unprotected surfaces in catalysis and electrocatalysis. Chem Sci 7:3188–3205. https://doi.org/10.1039/C5SC04714E

    CAS  Article  Google Scholar 

  3. Bai X, Gao Y, Liu H, Zheng L (2009) Synthesis of amphiphilic ionic liquids terminated gold nanorods and their superior catalytic activity for the reduction of nitro compounds. J Phys Chem C 113:17730–17736. https://doi.org/10.1021/jp906378d

    CAS  Article  Google Scholar 

  4. Balasubramanian SK, Yang L, Yung L-YL et al (2010) Characterization, purification, and stability of gold nanoparticles. Biomaterials 31:9023–9030. https://doi.org/10.1016/j.biomaterials.2010.08.012

    CAS  Article  Google Scholar 

  5. Biju V (2014) Chemical modifications and bioconjugate reactions of nanomaterials for sensing, imaging, drug delivery and therapy. Chem Soc Rev 43:744–764. https://doi.org/10.1039/C3CS60273G

    CAS  Article  Google Scholar 

  6. Binupriya AR, Sathishkumar M, Vijayaraghavan K, Yun S-I (2010) Bioreduction of trivalent aurum to nano-crystalline gold particles by active and inactive cells and cell-free extract of Aspergillus oryzae var. viridis. J Hazard Mater 177:539–545. https://doi.org/10.1016/j.jhazmat.2009.12.066

    CAS  Article  Google Scholar 

  7. Boone DR, Castenholz RW, Garrity GM (eds) (2001) Bergey’s manual of systematic bacteriology, 2nd edn. New York, Springer

    Google Scholar 

  8. Booth G (2000) Nitro compounds, aromatic. In: Wiley-VCH Verlag GmbH &Co. KGaA (ed) Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH Verlag GmbH &Co. KGaA, Weinheim, Germany

  9. Chakraborty A, Bera A, Mukherjee A et al (2015) Changing bacterial profile of Sundarbans, the world heritage mangrove: impact of anthropogenic interventions. World J Microbiol Biotechnol 31:593–610. https://doi.org/10.1007/s11274-015-1814-5

    CAS  Article  Google Scholar 

  10. Chirea M, Freitas A, Vasile BS et al (2011) Gold nanowire networks: synthesis, characterization, and catalytic activity. Langmuir 27:3906–3913. https://doi.org/10.1021/la104092b

    CAS  Article  Google Scholar 

  11. Chiu C-Y, Chung P-J, Lao K-U et al (2012) Facet-dependent catalytic activity of gold nanocubes, octahedra, and rhombic dodecahedra toward 4-nitroaniline reduction. J Phys Chem C 116:23757–23763. https://doi.org/10.1021/jp307768h

    CAS  Article  Google Scholar 

  12. Correa-Llantén DN, Muñoz-Ibacache SA, Castro ME et al (2013) Gold nanoparticles synthesized by Geobacillus sp. strain ID17 a thermophilic bacterium isolated from Deception Island, Antarctica. Microb Cell Fact 12:75. https://doi.org/10.1186/1475–2859–12-75

    Article  Google Scholar 

  13. Dahl JA, Maddux BLS, Hutchison JE (2007) Toward greener nanosynthesis. Chem Rev 107:2228–2269. https://doi.org/10.1021/cr050943k

    CAS  Article  Google Scholar 

  14. Das SK, Dickinson C, Lafir F et al (2012) Synthesis, characterization and catalytic activity of gold nanoparticles biosynthesized with Rhizopus oryzae protein extract. Green Chem 14:1322. https://doi.org/10.1039/c2gc16676c

    CAS  Article  Google Scholar 

  15. Dash SS, Bag BG (2014) Synthesis of gold nanoparticles using renewable Punica granatum juice and study of its catalytic activity. Appl Nanosci 4:55–59. https://doi.org/10.1007/s13204-012-0179-4

    CAS  Article  Google Scholar 

  16. Esumi K, Isono R, Yoshimura T (2004) Preparation of PAMAM– and PPI–metal (silver, platinum, and palladium) nanocomposites and their catalytic activities for reduction of 4-nitrophenol. Langmuir 20:237–243. https://doi.org/10.1021/la035440t

    CAS  Article  Google Scholar 

  17. Fan G-Y, Huang W-J (2014) Synthesis of ruthenium/reduced graphene oxide composites and application for the selective hydrogenation of halonitroaromatics. Chin Chem Lett 25:359–363. https://doi.org/10.1016/j.cclet.2013.11.044

    CAS  Article  Google Scholar 

  18. Fu A, Zhang E (2015) A new strategy for specific imaging of neural cells based on peptide-conjugated gold nanoclusters. Int J Nanomed 2115. doi: https://doi.org/10.2147/IJN.S78554

  19. Gangula A, Podila R, Rao M et al (2011) Catalytic reduction of 4-nitrophenol using biogenic gold and silver nanoparticles derived from Breynia rhamnoides. Langmuir 27:15268–15274. https://doi.org/10.1021/la2034559

    Article  Google Scholar 

  20. Gole A, Dash C, Ramakrishnan V et al (2001) Pepsin–gold colloid conjugates: preparation, characterization, and enzymatic activity. Langmuir 17:1674–1679. https://doi.org/10.1021/la001164w

    CAS  Article  Google Scholar 

  21. Guria MK, Majumdar M, Bhattacharyya M (2016) Green synthesis of protein capped nano-gold particle: an excellent recyclable nano-catalyst for the reduction of nitro-aromatic pollutants at higher concentration. J Mol Liq 222:549–557. https://doi.org/10.1016/j.molliq.2016.07.087

    CAS  Article  Google Scholar 

  22. He S, Guo Z, Zhang Y et al (2007) Biosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulata. Mater Lett 61:3984–3987. https://doi.org/10.1016/j.matlet.2007.01.018

    CAS  Article  Google Scholar 

  23. Hulkoti NI, Taranath TC (2014) Biosynthesis of nanoparticles using microbes—a review. Colloids Surf B Biointerfaces 121:474–483. https://doi.org/10.1016/j.colsurfb.2014.05.027

    CAS  Article  Google Scholar 

  24. Iravani S (2014) Bacteria in nanoparticle synthesis: current status and future prospects. Int Sch Res Notices 2014:1–18. https://doi.org/10.1155/2014/359316

    Article  Google Scholar 

  25. Jia H, Gao X, Chen Z et al (2012) The high yield synthesis and characterization of gold nanoparticles with superior stability and their catalytic activity. Cryst Eng Comm 14:7600. https://doi.org/10.1039/c2ce25840d

    CAS  Article  Google Scholar 

  26. Jiang H, Dong H, Zhang G et al (2006) Microbial diversity in water and sediment of Lake Chaka, an Athalassohaline Lake in northwestern China. Appl Environ Microbiol 72:3832–3845. https://doi.org/10.1128/AEM.02869-05

    CAS  Article  Google Scholar 

  27. Kannan P, Abraham John S (2008) Synthesis of mercaptothiadiazole-functionalized gold nanoparticles and their self-assembly on Au substrates. Nanotechnology 19:85602. https://doi.org/10.1088/0957-4484/19/8/085602

    Article  Google Scholar 

  28. Karthick V, Kumar VG, Dhas TS et al (2014) Effect of biologically synthesized gold nanoparticles on alloxan-induced diabetic rats—an in vivo approach. Colloids Surf B Biointerfaces 122:505–511. https://doi.org/10.1016/j.colsurfb.2014.07.022

    CAS  Article  Google Scholar 

  29. Kim BK, Lim Y-W, Kim M et al (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261. https://doi.org/10.1099/ijs.0.64915-0

    Article  Google Scholar 

  30. Kim JH, Park JH, Chung YK, Park KH (2012) Ruthenium nanoparticle-catalyzed, controlled and Chemoselective hydrogenation of nitroarenes using ethanol as a hydrogen source. Adv Synth Catal 354:2412–2418. https://doi.org/10.1002/adsc.201200356

    CAS  Article  Google Scholar 

  31. Lee J, Park JC, Bang JU, Song H (2008) Precise tuning of porosity and surface functionality in Au@SiO 2 nanoreactors for high catalytic efficiency. Chem Mater 20:5839–5844. https://doi.org/10.1021/cm801149w

    CAS  Article  Google Scholar 

  32. Li H, Gao S, Zheng Z, Cao R (2011) Bifunctional composite prepared using layer-by-layer assembly of polyelectrolyte–gold nanoparticle films on Fe3O4–silica core–shell microspheres. Catal Sci Technol 1:1194. https://doi.org/10.1039/c1cy00096a

    CAS  Article  Google Scholar 

  33. Lin C, Tao K, Hua D et al (2013) Size effect of gold nanoparticles in catalytic reduction of p-nitrophenol with NaBH4. Molecules 18:12609–12620. https://doi.org/10.3390/molecules181012609

    CAS  Article  Google Scholar 

  34. Lin W-H, Lu Y-H, Hsu Y-J (2014) Au nanoplates as robust, recyclable SERS substrates for ultrasensitive chemical sensing. J Colloid Interface Sci 418:87–94. https://doi.org/10.1016/j.jcis.2013.11.082

    CAS  Article  Google Scholar 

  35. Liu H, Yang Q (2011) Facile fabrication of nanoporous Au–Pd bimetallic foams with high catalytic activity for 2-nitrophenol reduction and SERS property. J Mater Chem 21:11961. https://doi.org/10.1039/c1jm10109a

    CAS  Article  Google Scholar 

  36. Mandlimath TR, Gopal B (2011) Catalytic activity of first row transition metal oxides in the conversion of p-nitrophenol to p-aminophenol. J Mol Catal A Chem 350:9–15. https://doi.org/10.1016/j.molcata.2011.08.009

    CAS  Article  Google Scholar 

  37. Manivasagan P, Alam MS, Kang K-H et al (2015) Extracellular synthesis of gold bionanoparticles by Nocardiopsis sp. and evaluation of its antimicrobial, antioxidant and cytotoxic activities. Bioprocess Biosyst Eng 38:1167–1177. https://doi.org/10.1007/s00449-015-1358-y

    CAS  Article  Google Scholar 

  38. Meena Kumari M, Jacob J, Philip D (2015) Green synthesis and applications of Au–Ag bimetallic nanoparticles. Spectrochim Acta A Mol Biomol Spectrosc 137:185–192. https://doi.org/10.1016/j.saa.2014.08.079

    CAS  Article  Google Scholar 

  39. Mohanpuria P, Rana NK, Yadav SK (2008) Biosynthesis of nanoparticles: technological concepts and future applications. J Nanopart Res 10:507–517. https://doi.org/10.1007/s11051-007-9275-x

    CAS  Article  Google Scholar 

  40. Nangia Y, Wangoo N, Goyal N et al (2009) A novel bacterial isolate Stenotrophomonas maltophilia as living factory for synthesis of gold nanoparticles. Microb Cell Factories 8:39. https://doi.org/10.1186/1475-2859-8-39

    Article  Google Scholar 

  41. Narayanan KB, Sakthivel N (2010) Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interf Sci 156:1–13. https://doi.org/10.1016/j.cis.2010.02.001

    CAS  Article  Google Scholar 

  42. Narayanan KB, Sakthivel N (2011) Synthesis and characterization of nano-gold composite using Cylindrocladium floridanum and its heterogeneous catalysis in the degradation of 4-nitrophenol. J Hazard Mater 189:519–525. https://doi.org/10.1016/j.jhazmat.2011.02.069

    CAS  Article  Google Scholar 

  43. Narayanan R, El-Sayed MA (2004) Shape-dependent catalytic activity of platinum nanoparticles in colloidal solution. Nano Lett 4:1343–1348. https://doi.org/10.1021/nl0495256

    CAS  Article  Google Scholar 

  44. Patra S, Mukherjee S, Barui AK et al (2015) Green synthesis, characterization of gold and silver nanoparticles and their potential application for cancer therapeutics. Mater Sci Eng C 53:298–309. https://doi.org/10.1016/j.msec.2015.04.048

    CAS  Article  Google Scholar 

  45. Pu Y-C, Wang G, Chang K-D et al (2013) Au nanostructure-decorated TiO2 nanowires exhibiting photoactivity across entire UV-visible region for photoelectrochemical water splitting. Nano Lett 13:3817–3823. https://doi.org/10.1021/nl4018385

    CAS  Article  Google Scholar 

  46. Rajan A, MeenaKumari M, Philip D (2014) Shape tailored green synthesis and catalytic properties of gold nanocrystals. Spectrochim Acta A Mol Biomol Spectrosc 118:793–799. https://doi.org/10.1016/j.saa.2013.09.086

    CAS  Article  Google Scholar 

  47. Reddy V, Torati RS, Oh S, Kim C (2013) Biosynthesis of gold nanoparticles assisted by Sapindus mukorossi Gaertn. Fruit pericarp and their catalytic application for the reduction of p-nitroaniline. Ind Eng Chem Res 52:556–564. https://doi.org/10.1021/ie302037c

    CAS  Article  Google Scholar 

  48. Sana B, Ghosh D, Saha M, Mukherjee J (2007) Purification and characterization of an extremely dimethylsulfoxide tolerant esterase from a salt-tolerant Bacillus species isolated from the marine environment of the Sundarbans. Process Biochem 42:1571–1578. https://doi.org/10.1016/j.procbio.2007.05.026

    CAS  Article  Google Scholar 

  49. Sengupta S, Pramanik A, Ghosh A, Bhattacharyya M (2015) Antimicrobial activities of actinomycetes isolated from unexplored regions of Sundarbans mangrove ecosystem. BMC Microbiol 15:170. https://doi.org/10.1186/s12866-015-0495-4

    Article  Google Scholar 

  50. Shankar SS, Rai A, Ankamwar B et al (2004) Biological synthesis of triangular gold nanoprisms. Nat Mater 3:482–488. https://doi.org/10.1038/nmat1152

    CAS  Article  Google Scholar 

  51. Sharma N, Pinnaka AK, Raje M et al (2012) Exploitation of marine bacteria for production of gold nanoparticles. Microb Cell Factories 11:86. https://doi.org/10.1186/1475-2859-11-86

    CAS  Article  Google Scholar 

  52. Sharma S (2015) Metal dependent catalytic hydrogenation of nitroarenes over water-soluble glutathione capped metal nanoparticles. J Colloid Interface Sci 441:25–29. https://doi.org/10.1016/j.jcis.2014.11.030

    CAS  Article  Google Scholar 

  53. Shen W, Qu Y, Pei X et al (2016) Green synthesis of gold nanoparticles by a newly isolated strain Trichosporon montevideense for catalytic hydrogenation of nitroaromatics. Biotechnol Lett 38:1503–1508. https://doi.org/10.1007/s10529-016-2120-5

    CAS  Article  Google Scholar 

  54. Shi C, Zhu N, Cao Y, Wu P (2015) Biosynthesis of gold nanoparticles assisted by the intracellular protein extract of Pycnoporus sanguineus and its catalysis in degradation of 4-nitroaniline. Nanoscale Res Lett 10:147. https://doi.org/10.1186/s11671-015-0856-9

    Article  Google Scholar 

  55. Singh C, Goyal A, Singhal S (2014) Nickel-doped cobalt ferrite nanoparticles: efficient catalysts for the reduction of nitroaromatic compounds and photo-oxidative degradation of toxic dyes. Nano 6:7959. https://doi.org/10.1039/c4nr01730g

    CAS  Google Scholar 

  56. Singha SS, Nandi D, Singha A (2015) Tuning the photoluminescence and ultrasensitive trace detection properties of few-layer MoS2 by decoration with gold nanoparticles. RSC Adv 5:24188–24193. https://doi.org/10.1039/C5RA01439E

    CAS  Article  Google Scholar 

  57. Sperling RA, Rivera Gil P, Zhang F et al (2008) Biological applications of gold nanoparticles. Chem Soc Rev 37:1896. https://doi.org/10.1039/b712170a

    CAS  Article  Google Scholar 

  58. Srivastava SK, Yamada R, Ogino C, Kondo A (2013) Biogenic synthesis and characterization of gold nanoparticles by Escherichia coli K12 and its heterogeneous catalysis in degradation of 4-nitrophenol. Nanoscale Res Lett 8:70. https://doi.org/10.1186/1556-276X-8-70

    Article  Google Scholar 

  59. Stalin Dhas T, Ganesh Kumar V, Stanley Abraham L et al (2012) Sargassum myriocystum mediated biosynthesis of gold nanoparticles. Spectrochim Acta A Mol Biomol Spectrosc 99:97–101. https://doi.org/10.1016/j.saa.2012.09.024

    CAS  Article  Google Scholar 

  60. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    CAS  Article  Google Scholar 

  61. Tan L, Chen D, Liu H, Tang F (2010) A silica nanorattle with a mesoporous shell: an ideal nanoreactor for the preparation of tunable gold cores. Adv Mater 22:4885–4889. https://doi.org/10.1002/adma.201002277

    CAS  Article  Google Scholar 

  62. Uma Suganya KS, Govindaraju K, Ganesh Kumar V et al (2015) Blue green alga mediated synthesis of gold nanoparticles and its antibacterial efficacy against Gram positive organisms. Mater Sci Eng C 47:351–356. https://doi.org/10.1016/j.msec.2014.11.043

    CAS  Article  Google Scholar 

  63. Vinay Gopal J, Thenmozhi M, Kannabiran K et al (2013) Actinobacteria mediated synthesis of gold nanoparticles using Streptomyces sp. VITDDK3 and its antifungal activity. Mater Lett 93:360–362. https://doi.org/10.1016/j.matlet.2012.11.125

    CAS  Article  Google Scholar 

  64. Weir RJ, Fisher RS (1972) Toxicologic studies on borax and boric acid. Toxicol Appl Pharmacol 23:351–364

    CAS  Article  Google Scholar 

  65. Wu C-C, Chen D-H (2012) Spontaneous synthesis of gold nanoparticles on gum arabic-modified iron oxide nanoparticles as a magnetically recoverable nanocatalyst. Nanoscale Res Lett 7:317. https://doi.org/10.1186/1556-276X-7-317

    Article  Google Scholar 

  66. Wu X-Q, Wu X-W, Huang Q et al (2015) In situ synthesized gold nanoparticles in hydrogels for catalytic reduction of nitroaromatic compounds. Appl Surf Sci 331:210–218. https://doi.org/10.1016/j.apsusc.2015.01.077

    CAS  Article  Google Scholar 

  67. Wunder S, Polzer F, Lu Y et al (2010) Kinetic analysis of catalytic reduction of 4-nitrophenol by metallic nanoparticles immobilized in spherical polyelectrolyte brushes. J Phys Chem C 114:8814–8820. https://doi.org/10.1021/jp101125j

    CAS  Article  Google Scholar 

  68. Zhan G, Huang J, Du M et al (2012) Liquid phase oxidation of benzyl alcohol to benzaldehyde with novel uncalcined bioreduction Au catalysts: high activity and durability. Chem Eng J 187:232–238. https://doi.org/10.1016/j.cej.2012.01.051

    CAS  Article  Google Scholar 

  69. Zhu C-H, Hai Z-B, Cui C-H et al (2012) In situ controlled synthesis of thermosensitive poly(N-isopropylacrylamide)/au nanocomposite hydrogels by gamma radiation for catalytic application. Small 8:930–936. https://doi.org/10.1002/smll.201102060

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the World Bank, for all the necessary support for the execution of ICZM project, West Bengal. Sudip Nag acknowledges World Bank ICZM project (54-ICZMP/3P) for providing his fellowship and financial support to carry out this work. Dr. Arnab Pramanik is supported by Research Associateship from NCSCM (MoEF, Govt. of India, grant no. 21/RCO/CR/CMR/2013). We would like to acknowledge the continuous encouragement and enthusiasm expressed by Mr. Tapas Paul and Dr. Herbert K. Acquay from the World Bank in our venture to explore the world heritage site, Sundarbans. We express our sincere gratitude to SPMU, NPMU, and IESWM for their continuous support. We are grateful to Prof. Parimal Karmakar, Jadavpur University, for his support during DLS and zeta potential measurements; Dr. Dipankar Das and Mr. Pallippuram Venkitaraman Rajesh, UGC-DAE, for their help in using XRD facility; Prof. Munna Sarkar, Saha Institute of Nuclear Physics, for her support during FTIR data analysis; and Dr. Subrata Kundu, CSIR-Central Electrochemical Research Institute for the valuable discussion. We are grateful to Dr. Achintya Singha and Mr. Tara Shankar Bhattacharya, Bose Institute, for their active support in performing SERS measurement and analyzing the data. We like to acknowledge UGC-CAS, DST–FIST, DBT-IPLS, UGC-UPE in the Department of Biochemistry, University of Calcutta, and Centre for Research in Nanoscience and Nanotechnology (CRNN), University of Calcutta, for providing the instrumental facility and infrastructural support. It would not be possible to carry out this work without the help and support of the local people of the Sundarbans. We express our inability to acknowledge them individually.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maitree Bhattacharyya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Responsible editor: Santiago V. Luis

Electronic supplementary material

ESM 1

(DOCX 4982 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nag, S., Pramanik, A., Chattopadhyay, D. et al. Green-fabrication of gold nanomaterials using Staphylococcus warneri from Sundarbans estuary: an effective recyclable nanocatalyst for degrading nitro aromatic pollutants. Environ Sci Pollut Res 25, 2331–2349 (2018). https://doi.org/10.1007/s11356-017-0617-7

Download citation

Keywords

  • Bacterial intracellular protein
  • Gold nanoparticles
  • Recyclable catalysis
  • Nitro aromatic pollutants
  • Wastewater treatment