Skip to main content
Log in

Green Roccella phycopsis Ach. mediated silver nanoparticles: synthesis, characterization, phenolic content, antioxidant, antibacterial and anti-acetylcholinesterase capacities

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

In this study, we develop here for the first time an easy, eco-friendly method for synthesizing silver nanoparticles (AgNPs) using the lichen Roccella phycopsis. AgNPs formation was first determined by a color change of the lichen filtrate to brown, subsequent to addition of AgNO3 solution, and confirmed by a maximum absorbance peak at 425 nm in UV–vis spectrum. Scanning electron microscope images showed a spherical shape with a size distribution between 11 and 18 nm, while the elemental composition was elucidated by the energy dispersive X-ray spectroscopy. The chemical compounds responsible for reduction and stabilization of silver nanoparticles were detected by Frourier transform infrared spectroscopy analysis. The synthesized R. phycopsis silver nanoparticles displayed a strong antioxidant activity. Further, the antibacterial activity was more effective against Gram-negative than Gram-positive bacteria. Besides, the R. phycopsis-AgNPs were potent in inhibiting acetylcholinesterase enzyme with IC50 value of 1.65 ± 0.07 mg/mL.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Aydin S, Kinalioğlu K (2016) Comparison of antioxidant activity of Roccella phycopsis Ach. (Roccellaceae) and Flavoparmelia caperata L. Hale (Parmeliaceae) lichens. Düzce Univ J Sci Technol 4:837–847

    Google Scholar 

  2. Aydin S, Kinalioğlu K (2013) The investigation of antibacterial activities of ethanol and methanol extracts of Flavoparmelia caperata (L.) Hale (Parmeliaceae) and Roccella phycopsis Ach. (Roccellaceae) lichens collected from Eastern Blacksea Region, Turkey. J Appl Pharm Sci 3:143–147. https://doi.org/10.7324/JAPS.2013.30225

    Article  Google Scholar 

  3. Fiorentino J (2015) Clarification regarding old records of Roccella in the Maltese Islands. Mycosphere 6:673–680

    Article  Google Scholar 

  4. Yalçın E, Çavuȿoğlu K, Kınalıoğlu K (2010) Biosorption of Cu2+ and Zn2+ by raw and autoclaved Rocella phycopsis. J Environ Sci 22:367–373. https://doi.org/10.1016/S1001-0742(09)60117-0

    Article  CAS  Google Scholar 

  5. Mie R, Din LB, Samsudin MW, Ahmad A (2014) Secondary metabolite isolated from Ramalina dumeticola and its application for silver nanoparticles production. AIP Conf Proc 1614:213–217. https://doi.org/10.1063/1.4895198

    Article  CAS  Google Scholar 

  6. Pirtarighat S, Ghannadnia M, Baghshahi S (2019) Biosynthesis of silver nanoparticles using Ocimum basilicum cultured under controlled conditions for bactericidal application. Mater Sci Eng C 98:250–255. https://doi.org/10.1016/j.msec.2018.12.090

    Article  CAS  Google Scholar 

  7. Das G, Patra JK, Shin H (2020) Biosynthesis, and potential effect of fern mediated biocompatible silver nanoparticles by cytotoxicity, antidiabetic, antioxidant and antibacterial, studies. Mater Sci Eng C 114:111011. https://doi.org/10.1016/j.msec.2020.111011

    Article  CAS  Google Scholar 

  8. Gopu M, Kumar P, Selvankumar T, Senthilkumar B, Sudhakar C, Govarthanan M, Kumar RS, Selvam K (2020) Green biomimetic silver nanoparticles utilizing the red algae Amphiroa rigida and its potent antibacterial, cytotoxicity and larvicidal efficiency. Bioprocess Biosyst Eng 44:217–223. https://doi.org/10.1007/s00449-020-02426-1

    Article  CAS  PubMed  Google Scholar 

  9. Khan AU, Malik N, Khan M, Cho MH, Khan MM (2017) Fungi-assisted silver nanoparticle synthesis and their applications. Bioprocess Biosyst Eng 41:1–20. https://doi.org/10.1007/s00449-017-1846-3

    Article  CAS  PubMed  Google Scholar 

  10. Küp FÖ, Çoȿkunçay S, Duman F (2019) Biosynthesis of silver nanoparticles using leaf extract of Aesculus hippocastanum (horse chestnut): evaluation of their antibacterial, antioxidant and drug release system activities. Mater Sci Eng C 107:110207. https://doi.org/10.1016/j.msec.2019.110207

    Article  CAS  Google Scholar 

  11. David L, Moldovana B, Baldea I, Olteanu D, Bolfa P, Clichici S, Filip GA (2020) Modulatory effects of Cornus sanguinea L mediated green synthesized silver nanoparticles on oxidative stress, COX-2/NOS2 and NFkB/pNFkB expressions in experimental inflammation in Wistar rats. Mater Sci Eng C 110:110709. https://doi.org/10.1016/j.msec.2020.110709

    Article  CAS  Google Scholar 

  12. Khan MM, Lee J, Cho MH (2014) Au@TiO2 nanocomposites for the catalytic degradation of methyl orange and methylene blue: an electron relay effect. J Ind Eng Chem 20:1584–1590. https://doi.org/10.1016/j.jiec.2013.08.002

    Article  CAS  Google Scholar 

  13. Korkmaz N, Ceylan Y, Hamid A, Karadağ A, Bülbül AS, Aftab MN, Çevik Ö, Şen F (2020) Biogenic silver nanoparticles synthesized via Mimusops elengi fruit extract, a study on antibiofilm, antibacterial, and anticancer activities. J Drug Deliv Sci Technol 59:101864. https://doi.org/10.1016/j.jddst.2020.101864

    Article  CAS  Google Scholar 

  14. Din LB, Mie R, Samsudin MW, Ahmad A, Ibrahim N (2015) Biometric synthesis of silver nanoparticles using the lichen Ramalina dumeticola and the antibacterial activity. Malaysian J Anal Sci 19:369–376

    Google Scholar 

  15. Siddiqi KS, Rashid M, Rahman A, Tajuddin HA, Rehman S (2018) Biogenic fabrication and characterization of silver nanoparticles using aqueous ethanolic extract of lichen (Usnea longissima) and their antimicrobial activity. Biomater Res 22:23. https://doi.org/10.1186/s40824-018-0135-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Mie R, Samsudin MW, Din LB, Ahmad A, Ibrahim N, Adnan SNA (2014) Synthesis of silver nanoparticles with antibacterial activity using the lichen Parmotrema praesorediosum. Int J Nanomedicine 9:121–127

    Article  Google Scholar 

  17. Sanchooli N, Saeidi S, Barani HK, Sanchooli E (2018) In vitro antibacterial effects of silver nanoparticles synthesized using Verbena officinalis leaf extract on Yersinia ruckeri, Vibrio cholera and Listeria monocytogenes. Iranian J Microbiol 10:400–408

    Google Scholar 

  18. Khan MM, Kalathil S, Lee J, Cho MH (2012) Synthesis of cysteine capped silver nanoparticles by electrochemically active biofilm and their antibacterial activities. Bull Korean Chem Soc 33:2592–2596. https://doi.org/10.5012/bkcs.2012.33.8.2592

    Article  CAS  Google Scholar 

  19. Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Meth Enzymol 299:152–178. https://doi.org/10.1016/S0076-6879(99)99017-1

    Article  CAS  Google Scholar 

  20. Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014. https://doi.org/10.1021/jf0115589

    Article  CAS  PubMed  Google Scholar 

  21. Adedapo AA, Jimoh FO, Koduru S, Afolayan AJ, Masika PJ (2008) Antibacterial and antioxidant properties of the methanol extracts of the leaves and stems of Calpurnia aurea. BMC Complement Altern Med 8:53. https://doi.org/10.1186/1472-6882-8-53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sun B, Ricardo-da-Silva JM, Spranger I (1998) Critical factors of vanillin assay for catechins and proanthocyanidins. J Agric Food Chem 46:4267–4274. https://doi.org/10.1021/jf980366j

    Article  CAS  Google Scholar 

  23. Porter LJ, Hrstich LN, Chan BG (1985) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230. https://doi.org/10.1016/S0031-9422(00)94533-3

    Article  Google Scholar 

  24. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss U Technol 28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5

    Article  CAS  Google Scholar 

  25. Koncic MZ, Petlevski R, Kalodera Z (2013) Antioxidant activity of Ipomoea batatas L. Lam. leaf grown in continental croatia and its effect on glutathione level in glucose-induced oxidative stress. Int J Food Prop 16:964–973. https://doi.org/10.1080/10942912.2011.573117

    Article  CAS  Google Scholar 

  26. Dinis TCP, Madeira VMC, Almeida LM (1994) Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch Biochem Biophys 315:161–169. https://doi.org/10.1006/abbi.1994.1485

    Article  CAS  PubMed  Google Scholar 

  27. NCCLS (1997) Performance standards for antimicrobial disk susceptibility tests. Approved standard M2–A6. Wayne. https://ci.nii.ac.jp/naid/10025861215/.

  28. Cosentino S, Tuberoso CIG, Pisano B, Satta M, Mascia V, Arzedi E, Palmas F (1999) In-vitro antimicrobial activity and chemical composition of Sardinian Thymus essential oils. Lett Appl Microbiol 29:130–135. https://doi.org/10.1046/j.1472-765X.1999.00605.x

    Article  CAS  PubMed  Google Scholar 

  29. Khadri A, Serralheiro MLM, Nogueira JMF, Neffati M, Smiti S, Araújo MEM (2008) Antioxidant and antiacetylcholinesterase activities of essential oils from Cymbopogon schoenanthus L. Spreng. Determination of chemical composition by GC–mass spectrometry and 13C NMR. Food Chem 109:630–637. https://doi.org/10.1016/j.foodchem.2007.12.070

    Article  CAS  Google Scholar 

  30. Khandel P, Kumar SS, Kanwar L, Kumar YR, Kumar SD (2018) Biochemical profiling of microbes inhibiting silver nanoparticles using symbiotic organisms. Int J Nano dimens 9:273–285

    CAS  Google Scholar 

  31. Alqahtani MA, Al Othman MR, Mohammed AE (2020) Biofabrication of silver nanoparticles with antibacterial and cytotoxic abilities using lichens. Sci Rep 10:16781. https://doi.org/10.1038/s41598-020-73683-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Khan MM, Ansari SA, Cho MH (2013) Novel Ag@TiO2 nanocomposite synthesized by electrochemically active biofilm for nonenzymatic hydrogen peroxide sensor. Mater Sci Eng C 33:4692–4699. https://doi.org/10.1016/j.msec.2013.07.028

    Article  CAS  Google Scholar 

  33. Yousaf H, Mehmood A, Ahmad KS, Raffi M (2020) Green synthesis of silver nanoparticles and their applications as an alternative antibacterial and antioxidant agents. Mater Sci Eng C 112:110901. https://doi.org/10.1016/j.msec.2020.110901

    Article  CAS  Google Scholar 

  34. Jebril S, Ben Jenana RK, Dridi C (2020) Green synthesis of silver nanoparticles using Melia azedarach leaf extract and their antifungal activities: In vitro and in vivo. Mater Chem Phys 248:122898. https://doi.org/10.1016/j.matchemphys.2020.122898

    Article  CAS  Google Scholar 

  35. Awwad AM, Salem MN, Aqarbeh MM, Abdulaziz FM (2020) Green synthesis, characterization of silver sulfide nanoparticles and antibacterial activity evaluation. Chem Int 6:42–48. https://doi.org/10.5281/zenodo.3243157

    Article  CAS  Google Scholar 

  36. Albeladi SSR, Malik MA, Al-thabaiti SA (2020) Facile biofabrication of silver nanoparticles using Salvia officinalis leaf extract and its catalytic activity towards Congo red dye degradation. J Mater Res Technol 9:10031–10044. https://doi.org/10.1016/j.jmrt.2020.06.074

    Article  CAS  Google Scholar 

  37. Dasari S, Suresh KA, Rajesh M, Reddy CSS, Hemalatha CS, Wudayagiri R, Valluru L (2013) Biosynthesis, characterization, antibacterial and antioxidant activity of silver nanoparticles produced by lichens. J Bionanosci 7:237–244. https://doi.org/10.1166/jbns.2013.1140

    Article  CAS  Google Scholar 

  38. Spencer HM, Buckman J, Foster AM, Kennedy CJ (2018) Compositional analysis by P-XRF and SEM-EDX of medieval window glass from Elgin Cathedral, Northern Scotland. Archaeometry 60:1018–1035. https://doi.org/10.1111/arcm.12357

    Article  CAS  Google Scholar 

  39. Kambale EK, Nkanga CI, Mutonkole BI, Bapolisi AM, Tassa DO, Liesse JI, Krause RMW, Memvanga PB (2020) Green synthesis of antimicrobial silver nanoparticles using aqueous leaf extracts from three Congolese plant species (Brillantaisia patula, Crossopteryx febrifuga and Senna siamea). Heliyon 6:e04493. https://doi.org/10.1016/j.heliyon.2020.e04493

    Article  PubMed  PubMed Central  Google Scholar 

  40. John MS, Nagoth JA, Ramasamy KP, Mancini A, Giuli G, Natalello A, Ballarini P, Miceli C, Pucciarelli S (2020) Synthesis of bioactive silver nanoparticles by a Pseudomonas strain associated with the Antarctic psychrophilic protozoan Euplotes focardii. Mar Drugs 18:38. https://doi.org/10.3390/md18010038

    Article  CAS  PubMed Central  Google Scholar 

  41. Calcott MJ, Ackerley DF, Knight A, Keyzers RA, Owen JG (2018) Secondary metabolism in the lichen symbiosis. Chem Soc Rev 47:1730–1760. https://doi.org/10.1039/C7CS00431A

    Article  CAS  PubMed  Google Scholar 

  42. Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep 25:188–200. https://doi.org/10.1039/B606983P

    Article  PubMed  Google Scholar 

  43. Aoussar N, Rhallabi N, Mhand RA, Manzali R, Bouksaim M, Douira A, Mellouki F (2018) Seasonal variation of antioxidant activity and phenolic content of Pseudevernia furfuracea, Evernia prunastri and Ramalina farinacea from Morocco. J Saudi Soc Agric Sci 19:1–6. https://doi.org/10.1016/j.jssas.2018.03.004

    Article  Google Scholar 

  44. Khan MM, Ansari SA, Amal MI, Lee J, Cho MH (2013) Highly visible light active Ag@TiO2 nanocomposites synthesized using an electrochemically active biofilm: a novel biogenic approach. Nanoscale 5:4427–4435. https://doi.org/10.1039/C3NR00613A

    Article  CAS  PubMed  Google Scholar 

  45. Khan AU, Khan M, Khan MM (2019) Antifungal and Antibacterial Assay by Silver Nanoparticles Synthesized from Aqueous Leaf Extract of Trigonella foenum-graecum. BioNanoSci 9:597–602. https://doi.org/10.1007/s12668-019-00643-x

    Article  Google Scholar 

  46. Ulagesan S, Nam TJ, Choi YH (2021) Préparation biogénique et caractérisation des nanoparticules d’argent Pyropia yezoensis (P.y AgNPs) et de leur activité antibactérienne contre Pseudomonas aeruginosa. Bioprocess Biosyst Eng 44:443–452. https://doi.org/10.1007/s00449-020-02454-x

    Article  CAS  PubMed  Google Scholar 

  47. Mukherjeea PK, Kumar V, Mal M, Houghton PJ (2007) Acetylcholinesterase inhibitors from plants. J Phytomed 14:189–200. https://doi.org/10.1016/j.phymed.2007.02.002

    Article  CAS  Google Scholar 

  48. García-Ayllón MS, Small DH, Avila J, Sáez-Valer J (2011) Revisiting the role of acetylcholinesterase in Alzheimer’s disease: cross-talk with P-tau and β-amyloid. Front Mol Neurosci 4:22. https://doi.org/10.3389/fnmol.2011.00022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Heng L, Li C, Kim JC, Liu Y, Jung JS, Koh YJ, Hur JS (2003) Biruloquinone, an acetylcholinesterase inhibitor produced by lichen-forming fungus Cladonia macilenta. J Microbiol Biotechnol 23:161–166. https://doi.org/10.4014/jmb.1207.07016

    Article  CAS  Google Scholar 

  50. Mendili M, Bannour M, Araújo MEM, Aschi-Smiti S, Seaward MRD, Khadhri A (2019) Secondary metabolites and antioxidant capacity of the Tunisian lichen Diplochistes ocellatus (Ascomycota). Int J Med Mushrooms 21:817–823. https://doi.org/10.1615/intjmedmushrooms.2019031423

    Article  PubMed  Google Scholar 

  51. Thadhani VM, Naaz Q, Choudhary MI, Mesaik MA, Karunaratne V (2014) Enzyme inhibitory and immunomodulatory activities of the depsidone lobaric acid extracted from the lichen Heterodermia sp. J Natl Sci Found Sri Lanka 42:193–196. https://doi.org/10.4038/jnsfsr.v42i2.6988

    Article  CAS  Google Scholar 

  52. Reddya RG, Veeraval L, Maitra S, Chollet-Krugler M, Tomasi S, Lohézic-Le Dévéhat F, Boustie J, Chakravarty S (2016) Lichen-derived compounds show potential for central nervous system therapeutics. Phytomedicine 23:1527–1534. https://doi.org/10.1016/j.phymed.2016.08.010

    Article  CAS  Google Scholar 

  53. Mirzajani F, Motevali SM, Jabbari S, Siadat SOR, Sefidbakht Y (2017) Recombinant acetylcholinesterase purification and its interaction with silver nanoparticle. Protein Expr Purif 136:58–65. https://doi.org/10.1016/j.pep.2017.05.007

    Article  CAS  PubMed  Google Scholar 

  54. Popli D, Anil V, Subramanyam AB, Namratha MN, Ranjitha VR, Rao SN, Rai RV, Govindappa M (2018) Endophyte fungi, Cladosporium species-mediated synthesis of silver nanoparticles possessing in vitro antioxidant, anti-diabetic and anti-Alzheimer activity. Artif Cells Nanomed Biotechnol 46:676–683. https://doi.org/10.1080/21691401.2018.1434188

    Article  CAS  PubMed  Google Scholar 

  55. Šinko G, Vrček IV, Goessler W, Leitinger G, Dijanošić A, Miljanić S (2014) Alteration of cholinesterase activity as possible mechanism of silver nanoparticle toxicity. Environ Sci Pollut Res 21:1391–1400. https://doi.org/10.1007/s11356-013-2016-z

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are thankful to the Unity of Research for Vegetal Ecology at the University of El-Manar II, Faculty of Sciences for providing lab facilities. We are also thankful to the Tunisian National Oil Company (ETAP) for assistance for SEM.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

Authors

Contributions

MBS: conceptualization, methodology, formal analysis, investigation, interpretation, data curation, writing. CA: carried out the antibacterial activity experiments. AK: methodology, validation, resources, supervision, review and editing.

Corresponding author

Correspondence to Ayda Khadhri.

Ethics declarations

Conflict of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ben Salah, M., Aouadhi, C. & Khadhri, A. Green Roccella phycopsis Ach. mediated silver nanoparticles: synthesis, characterization, phenolic content, antioxidant, antibacterial and anti-acetylcholinesterase capacities. Bioprocess Biosyst Eng 44, 2257–2268 (2021). https://doi.org/10.1007/s00449-021-02601-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-021-02601-y

Keywords

Navigation