Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bacterial indoleacetic acid-induced synthesis of colloidal Ag2O nanocrystals and their biological activities

  • 108 Accesses

  • 3 Citations

Abstract

The biosynthesis and biological activity of colloidal Ag2O nanocrystals have not been well studied, although they have potential applications in many fields. For the first time, we developed a reducing agent free, cost-effective technique for Ag2O biosynthesis using Xanthomonas sp. P5. The optimal conditions for Ag2O synthesis were 50 °C, pH 8, and 2.5 mM AgNO3. Using these conditions the yield of Ag2O obtained at 10 h was about five times higher than that obtained at 12 h under unoptimized conditions. Ag2O was characterized by FESEM-EDS, TEM, dynamic light scattering, XRD, and UV–Visible spectroscopy. Indoleacetic acid produced by the strain P2 was involved in the synthesis of Ag2O. Ag2O exhibited a broad antimicrobial spectrum against several human pathogens. Furthermore, Ag2O exhibited 1,1-diphenyl-2-picrylhydrazyl (IC50 = 25.1 µg/ml) and 2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonate (IC50 = 16.8 µg/ml) radical scavenging activities, and inhibited collagenase (IC50 = 27.9 mg/ml). Cytotoxicity of Ag2O was tested in fibroblast cells and found to be non-toxic, demonstrating biocompatibility.

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

References

  1. 1.

    Manivasagan P, Nam SY, Oh J (2016) Marine microorganisms as potential biofactories for synthesis of metallic nanoparticles. Crit Rev Microbiol 42:1007–1019

  2. 2.

    Płaza GA, Chojniak J, Banat IM (2014) Biosurfactant mediated biosynthesis of selected metallic nanoparticles. Int J Mol Sci 15:13720–13737

  3. 3.

    Faramarzi MA, Sadighi A (2013) Insights into biogenic and chemical production of inorganic nanomaterials and nanostructures. Adv Colloid Interface Sci 189–190:1–20

  4. 4.

    Ali J, Zainab S, Ali N (2015) Green synthesis of metal nanoparticles by microorganisms; a current prospective. J Nanoanalysis 2:32–38

  5. 5.

    Rai M, Kon K, Ingle A, Duran N, Galdiero S, Galdiero M (2014) Broad-spectrum bioactivities of silver nanoparticles: the emerging trends and future prospects. Appl Microbiol Biotechnol 98:1951–1961

  6. 6.

    Parikh RY, Singh S, Prasad BLV, Patole MS, Sastry M, Shouche YS (2008) Extracellular synthesis of crystalline silver nanoparticles and molecular evidence of silver resistance from Morganella sp.: towards understanding biochemical synthesis mechanism. Chem BioChem 9:1415–1422

  7. 7.

    Bake S, Satish S (2015) Biosynthesis of gold nanoparticles by Pseudomonas veronii AS41G inhabiting Annona squamosa L. Spectrochim Acta A 150:691–695

  8. 8.

    Gaidhani SV, Yeshvekar RK, Shedbalkar UU, Bellare JH, Chopade BA (2014) Bio-reduction of hexachloroplatinic acid to platinum nanoparticles employing Acinetobacter calcoaceticus. Process Biochem 49:2313–2319

  9. 9.

    Ramanathan R, Field MR, O’Mullane AP, Smooker PM, Bhargava SK, Bansal V (2013) Aqueous phase synthesis of copper nanoparticles: a link between heavy metal resistance and nanoparticle synthesis ability in bacterial systems. Nanoscale 5:2300–2306

  10. 10.

    Wang T, Jin X, Chen Z, Megharaj M, Naidu R (2014) Green synthesis of Fe nanoparticles using eucalyptus leaf extracts for treatment of eutrophic wastewater. Sci Total Environ 466–467:210–213

  11. 11.

    Vijayakumar S, Vinoj G, Malaikozhundan B, Shanthi S, Vaseeharan B (2015) Plectranthus amboinicus leaf extract mediated synthesis of zinc oxide nanoparticles and its control of methicillin resistant Staphylococcus aureus biofilm and blood sucking mosquito larvae. Spectrochim Acta A 137:886–891

  12. 12.

    Choi Y, Park TJ, Lee DC, Lee SY (2018) Recombinant Escherichia coli as a biofactory for various single- and multi-element nanomaterials. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1804543115

  13. 13.

    Borase HP, Salunke BK, Salunkhe RB, Patil CD, Hallsworth JE, Kim BS, Patil SV (2014) Plant extract: a promising biomatrix for ecofriendly, controlled synthesis of silver nanoparticles. Appl Biochem Biotechnol 173:1–29

  14. 14.

    Ahmed S, Annu, Ikram S, Salprima Yudha S (2016) Biosynthesis of gold nanoparticles: a green approach. J Photochem Photobiol B 161:141–153

  15. 15.

    Thenmozhi M, Kannabiran K, Kumar R, Gopiesh Khanna V (2013) Antifungal activity of Streptomyces sp. VITSTK7 and its synthesized Ag2O/Ag nanoparticles against medically important Aspergillus pathogens. J Mycol Med 23:97–103

  16. 16.

    Varkey AJ, Fort AF (1993) Some optical properties of silver peroxide (AgO) and silver oxide (Ag2O) films produced by chemical-bath deposition. Sol Energy Mater Sol Cell 29:253–259

  17. 17.

    Peyser LA, Vinson AE, Bartko AP, Dickson RM (2001) Photo-activated fluorescence from individual silver nanoclusters. Science 291:103–106

  18. 18.

    Parkhurst WA, Dallek S, Larrick BF (1984) Thermogravimetry-evolved gas analysis of silver oxide cathode material. J Electrochem Soc 131:1739–1742

  19. 19.

    Sangappa M, Thiagarajan P (2015) Combating drug resistant pathogenic bacteria isolated from clinical infection, with silver oxide nanoparticles. Ind J Pharm Sci 77:151–155

  20. 20.

    Wei W, Mao X, Ortiz LA, Sadpaway DY (2011) Oriented silver oxide nanostructures synthesized through a template-free electrochemical route. J Mater Chem 21:432–438

  21. 21.

    Dhoondia ZH, Chakraborty H (2013) Lactobacillus mediated synthesis of silver oxide nanoparticles. Nanomater Nanotechnol 2:1–7

  22. 22.

    Karunakaran G, Jagathambal M, Gusev A, Minh NV, Kolesnikov E, Mandal AR, Kuznetsov D (2016) Nitrobacter sp. extract mediated biosynthesis of Ag2O NPs with excellent antioxidant and antibacterial potential for biomedical application. IET Nanobiotechnol 10:425–430

  23. 23.

    Ravichandran S, Paluri V, Loganathan GKK, Venkata BRK (2016) A novel approach for the biosynthesis of silver oxide nanoparticles using aqueous leaf extract of Callistemon lanceolatus (Myrtaceae) and their therapeutic potential. J Exp Nanosci 11:445–458

  24. 24.

    Cloud JE, Taylor LW, Yang Y (2014) A simple and effective method for controllable synthesis of silver and silver oxide nanocrystals. RSC Adv 4:24551–24559

  25. 25.

    Gopinath V, Velusamy P (2013) Extracellular biosynthesis of silver nanoparticles using Bacillus sp. GP-23 and evaluation of their antifungal activity towards Fusarium oxysporum. Spectrochim Acta A 106:170–174

  26. 26.

    Kalimuthu K, Babu RS, Venkataraman D, Bilal M, Gurunathan S (2008) Biosynthesis of silver nanocrystals by Bacillus licheniformis. Colloids Surf B 65:150–153

  27. 27.

    Jeong JH, Park KH, Oh DJ, Hwang DY, Kim HS, Lee CY, Son HJ (2010) Keratinolytic enzyme-mediated biodegradation of recalcitrant feather by a newly isolated Xanthomonas sp. P5. Polym Degrad Stab 95:1969–1977

  28. 28.

    Narayanan KB, Sakthivel N (2013) Biosynthesis of silver nanoparticles by phytopathogen Xanthomonas oryzae pv. oryzae strain BXO8. J Microbiol Biotechnol 23:1287–1292

  29. 29.

    Harley SM (1993) Use of a simple, colorimetric assay to demonstrate conditions for induction of nitrate reductase in plant. Am Biol Teach 55:161–164

  30. 30.

    Tang YW, Bonner J (1947) The enzymatic inactivation of indoleacetic acid I. Some characteristics of the enzyme contained in pea seedlings. Arch Biochem 13:17–25

  31. 31.

    Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–2100

  32. 32.

    Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

  33. 33.

    Mandl I, Keller S, Manahan J (1964) Multiplicity of Clostridium histolyticum collagenases. Biochemistry 3:1737–1741

  34. 34.

    Mie G (1908) Contribution to the optics of turbid media, particularly of colloidal metal solutions. Ann Phys 25:377–445

  35. 35.

    Nayak RR, Pradhan N, Behera D, Pradhan KM, Mishra S, Sukla LB, Mishra BK (2011) Green synthesis of silver nanoparticle by Penicillium purpurogenum NPMF: the process and optimization. J Nanopart Res 13:3129–3137

  36. 36.

    Kathiresan K, Manivannan S, Nabeel MA, Dhivya B (2009) Studies on silver nanoparticles synthesized by a marine fungus, Penicillium fellutanum isolated from coastal mangrove sediment. Colloids Surf B 71:133–137

  37. 37.

    Gurunathan S, Kalishwaralal K, Vaidyanathan R, Rail MK (2009) Biosynthesis, purification and characterization of silver nanoparticles using Escherichia coli. Colloids Surf B 74:328–335

  38. 38.

    Bankar AV, Joshi BS, Kumar AR, Zinjarde SS (2010) Banana peel extract mediated synthesis of gold nanoparticles. Colloids Surf B 80:45–50

  39. 39.

    Annamalai J, Nallamuthu T (2016) Green synthesis of silver nanoparticles: characterization and determination of antibacterial potency. Appl Nanosci 6:259–265

  40. 40.

    Zhou W, Liu H, Wang J, Liu D, Du G, Cui J (2010) Ag2O/TiO2 nanobelts heterostructure with enhanced ultraviolet and visible photocatalytic activity. ACS Appl Mater Interfaces :2385–2392

  41. 41.

    Kulkarni RR, Shaiwale NS, Deobagkar DN, Deobagkar DD (2015) Synthesis and extracellular accumulation of silver nanoparticles by employing radiation-resistant Deinococcus radiodurans, their characterization, and determination of bioactivity. Int J Nanomed 10:963–974

  42. 42.

    Sanghi R, Verma p (2009) Biomimetic synthesis and characterisation of protein capped silver nanoparticles. Bioresour Technol 100:501–504

  43. 43.

    Dong A, Huang P, Caughey B, Caughey WS (1995) Infrared analysis of ligand- and oxidation-induced conformational changes in hemoglobins and myoglobins. Arch Biochem Biophys 316:893–898

  44. 44.

    Elemike EE, Onwudiwe DC, Ekennia AC, Sonde CU, Ehiri RC (2017) Green synthesis of Ag/Ag2O nanoparticles using aqueous leaf extract of Eupatorium odoratum and its antimicrobial and mosquito larvicidal activities. Molecules 22:674–688

  45. 45.

    Durán N, Marcato PD, Durán M, Yadav A, Gade A (2011) Mechanistic aspects in the biogenic synthesis of extracellular metal nanoparticles by peptides, bacteria, fungi, and plants. Appl Microbiol Biotechnol 90:1609–1624

  46. 46.

    Priyadarshini S, Gopinath V, Meera PN, MubarakAli D, Velusamy P (2013) Synthesis of anisotropic silver nanoparticles using novel strain, Bacillus flexus and its biomedical application. Colloids Surf B 102:232–237

  47. 47.

    Sullivan KT, Wu C, Piekiel NW, Gaskell K, Zachariah MR (2013) Synthesis and reactivity of nano-Ag2O as an oxidizer for energetic systems yielding antimicrobial products. Combust Flame 160:438–446

  48. 48.

    Vithiya K (2015) Bacteria mediated extracellular synthesis and biological applications of silver oxide nanoparticles. PhD Thesis, VIT University, India

  49. 49.

    Harish BS, Uppuluri KB, Anbazhagan V (2010) Synthesis of fibrinolytic active silver nanoparticle using wheat bran xylan as a reducing and stabilizing agent. Carbohydr Polym 132:104–110

  50. 50.

    Seralathan J, Stevenson P, Subramaniam S, Raghavan R, Pemaiah B, Sivasubramanian A, Veerappan A (2014) Spectroscopy investigation on chemo-catalytic, free radical scavenging and bactericidal properties of biogenic silver nanoparticles synthesized using Salicornia brachiata aqueous extract. Spectrochim Acta A 118:349–355

  51. 51.

    Gahlawat G, Shikha S, Chaddha BS, Chaudhuri SR, Mayilraj S, Choudhury AR (2016) Microbial glycolipoprotein-capped silver nanoparticles as emerging antibacterial agents against cholera. Microb Cell Fact 15:25–39

  52. 52.

    Ramamurthy CH, Padma M, Samadanam IDM, Mareeswaran R, Suyavaran A, Kumar MS, Premkumar K, Thirunavukkarasu C (2013) The extra cellular synthesis of gold and silver nanoparticles and their free radical scavenging and antibacterial properties. Colloids Surf B 102:808–815

  53. 53.

    Juskova M, Majekova M, Demopoulos V, Stefek M (2011) Substituted derivatives of indole acetic acid as aldose reductase inhibitors with antioxidant activity: structure-activity relationship. Gen Physiol Biophys 30:342–349

  54. 54.

    Acard MES, Chen KW, Sweet MJ, Watts RE, Schroder K, Schembr MA, McEwan AG (2013) An antioxidant role for catecholate siderophores in Salmonella. Biochem J 454:543–549

  55. 55.

    Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

  56. 56.

    Mukherjee PK, Maitya N, Nema NK, Sarkar BK (2001) Bioactive compounds from natural resources against skin aging. Phytomedicine 19:64–73

  57. 57.

    Thring TSA, Hili P, Naughton DP (2009) Anti-collagenase, anti-elastase and anti-oxidant activities of extracts from 21 plants. BMC Complement Altern Med 9:27–38

  58. 58.

    Raffetto RD, Khalil A (2008) Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 75:346–359

  59. 59.

    Kanade S, Nataraj G, Ubale M, Mehta P (2016) Fluorescein diacetate vital staining for detecting viability of acid-fast bacilli in patients on antituberculosis treatment. Int J Mycobacteriol 6:294–298

Download references

Acknowledgements

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A1A01056919).

Author information

Correspondence to Hong-Joo Son.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 848 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yoo, J., Jang, E., Jeong, S. et al. Bacterial indoleacetic acid-induced synthesis of colloidal Ag2O nanocrystals and their biological activities. Bioprocess Biosyst Eng 42, 401–414 (2019). https://doi.org/10.1007/s00449-018-2044-7

Download citation

Keywords

  • Ag2O nanocolloids
  • Antimicrobial activity
  • Collagenase inhibition
  • Indoleacetic acid
  • Xanthomonas sp