Comparison of antibacterial and antibiofilm activities of biologically synthesized silver nanoparticles against several bacterial strains of medical interest

Abstract

Biological routes have been extensively explored in the synthesis of metallic nanoparticles due to their simplicity and low cost. Among metallic nanoparticles, silver nanoparticles (AgNPs) are widely used in medical applications because of their potent antimicrobial activity. In this work, the ability of the mycelium-free fungus extract produced by Chilean white-root Stereum hirsutum and two plant extracts (green tea and dill) were used in the synthesis of AgNPs. The synthesized nanoparticles were extensively characterized by different techniques. The antibacterial activity of the nanoparticles was demonstrated against the Gram-positive strain Staphylococcus aureus ATCC 29213 and Enterococcus faecalis ATCC 3229 (standard CLSI); and the Gram-negative bacterial strains (standard CLSI) Escherichia coli ATCC 25922, Klebsiella pneumoniae ATCC 13803 and the multidrug-resistant Pseudomonas aeruginosa KPC 37. The values of minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) were obtained in the range of 1.56–25 µg mL⁻¹. AgNPs synthesized by dill extract showed lower values of MIC and MBC, compared to other nanoparticles. The potent antibiofilm ability of AgNPs was demonstrated, including against the multidrug-resistant P. aeruginosa KPC 37 strain. All synthesized nanoparticles demonstrated antibiofilm activity. AgNPs synthesized by fungus extract demonstrated superior antibiofilm activity, compared to AgNPs synthesized by green tea or dill, at low concentration (1.56 µg mL⁻¹). To our best knowledge, this is the first report to compare the antioxidant and antibacterial effects of AgNPs synthesized by different biological entities (green tea, dill and S. hirsutum) with great importance in the combat of resistant bacteria and biofilms.

Keywords

Silver nanoparticles / Biogenic synthesis / Stereum hirsutum / Antibacterial / Antioxidant activity / Antibiofilm

References

[1] Ali SG, Ansari MA, Khan HM, Jalal M, Mahdi AA, Cameotra SS. Antibacterial and antibiofilm potential of green synthesized silver nanoparticles against Imipenem resistant clinical isolates of Pseudomonas aeruginosa. Bionanoscience, 2018, 8: 544-553

[2] Alsammarraie FK, Wang W, Zhou P, Mustapha A, Lin M. Green synthesis of silver nanoparticles using turmeric extracts and investigation of their antibacterial activities. Colloids Surf B Biointerfaces, 2018, 171: 398-405

[3] Ansari Z, Saha A, Singha SS, Sen K. Phytomediated generation of Ag, CuO and Ag-Cu nanoparticles for dimethoate sensing. J Photochem Photobiol A Chem, 2018, 367: 200-211

[4] Asghar MA, Zahir E, Shahid SM, Khan MN, Asghar MA, Iqbal J, Walker G. Iron, copper and silver nanoparticles: green synthesis using green and black tea leaves extracts and evaluation of antibacterial, antifungal and aflatoxin B1 adsorption activity. LWT-Food Sci Technol, 2018, 90: 98-107

[5] Baber R, Mazzei L, Thanh NTK, Gavriilidis A. An engineering approach to synthesis of gold and silver nanoparticles by controlling hydrodynamics and mixing based on a coaxial flow reactor. Nanoscale, 2017, 9: 14149-14161

[6] Basavaraja S, Balaji SD, Lagashetty A, Rajasab AH. Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium semitectum. Mater Res Bull, 2008, 43: 1164-1170

[7] Cuevas R, Durán N, Diez MC, Tortella GR, Rubilar O. Extracellular biosynthesis of copper and copper oxide nanoparticles by Stereum hirsutum, a native white-rot fungus from Chilean forests. J Nanomater, 2015, 10: 1-7

[8] de Lima R, Seabra AB, Durán N. Silver nanoparticles : a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J Appl Toxicol, 2012, 32: 867-879

[9] de Oliveira Silva BS, Seabra AB. Characterization of iron nanoparticles produced with green tea extract: a promising material for nitric oxide delivery. Biointerface Res Appl Chem, 2016, 6: 1280-1287

[10] Dubey SP, Lahtinen M, Sillanpää M. Green synthesis and characterizations of silver and gold nanoparticles using leaf extract of Rosa rugosa. Colloids Surf A Physicochem Eng Asp, 2010, 364: 34-41

[11] Duran N, Seabra AB. Biogenic synthesized Ag/Au nanoparticles: production, characterization, and applications. Curr Nanosci, 2018, 14: 82-94

[12] Durán N, Marcato PD, Alves OL, De Souza GIH, Esposito E. Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. J Nanobiotechnol, 2005, 3: 1-7

[13] Durán N, Durán M, de Jesus MB, Seabra AB, Fávaro WJ, Nakazato G. Silver nanoparticles: a new view on mechanistic aspects on antimicrobial activity. Nanomedicine, 2016, 12: 789-799

[14] Durán N, Nakazato G, Seabra AB. Antimicrobial activity of biogenic silver nanoparticles, and silver chloride nanoparticles: an overview and comments. Appl Microbiol Biotechnol, 2016, 100: 6555-6570

[15] Ebrahiminezhad A, Zare-Hoseinabadi A, Sarmah AK, Taghizadeh S, Ghasemi Y, Berenjian A. Plant-mediated synthesis and applications of iron nanoparticles. Mol Biotechnol, 2018, 60: 154-168

[16] Fahimirad S, Ajalloueian F, Ghorbanpour M. Synthesis and therapeutic potential of silver nanomaterials derived from plant extracts. Ecotoxicol Environ Saf, 2019, 168: 260-278

[17] Fernández JG, Fernández-Baldo MA, Berni E, Camí G, Durán N, Raba J, Sanz MI. Production of silver nanoparticles using yeasts and evaluation of their antifungal activity against phytopathogenic fungi. Process Biochem, 2016, 51: 1306-1313

[18] Fierascu RC, Ion RM, Dumitriu I. Noble metals nanoparticles synthesis in plant extracts. Optoelectron Adv Mater Rapid Commun, 2010, 4: 1297-1300

[19] Flores-López LZ, Espinoza-Gómez H, Somanathan R. Silver nanoparticles: electron transfer, reactive oxygen species, oxidative stress, beneficial and toxicological effects Mini review. J Appl Toxicol, 2019, 39: 16-26

[20] Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Hoiby N, Molin S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol, 2012, 10: 841-851

[21] Furusawa C, Horinouchi T, Maeda T. Toward prediction and control of antibiotic-resistance evolution. Curr Opin Biotechnol, 2018, 54: 45-49

[22] Garg S, Garg A. Encapsulation of curcumin in silver nanoparticle for enhancement of anticancer drug delivery. Int J Pharm Sci Res, 2018, 9: 1160-1166

[23] Guo C, Zhou L, Lv J. Effects of expandable graphite and modified ammonium polyphosphate on the flame-retardant and mechanical properties of wood flour-polypropylene composites. Polym Polym Compos, 2013, 21: 449-456

[24] Gurunathan S, Han JW, Kwon DN, Kim JH. Enhanced antibacterial and anti-biofilm activities of silver nanoparticles against gram-negative and gram-positive bacteria. Nanoscale Res Lett, 2014, 9: 1-17

[25] Han L, Wang P, Zhu C, Zhai Y, Dong S. Facile solvothermal synthesis of cube-like Ag@AgCl: a highly efficient visible light photocatalyst. Nanoscale, 2011, 3: 2931-2935

[26] Ignat I, Volf I, Popa VI. A critical review of methods for characterisation of polyphenolic compounds in fruits and vegetables. Food Chem, 2011, 126: 1821-1835

[27] Jeukens J, Boyle B, Kukavica-Ibrulj I, Ouellet MM, Aaron SD, Charette SJ, Fothergill JL, Tucker NP, Winstanley C, Levesque RC. Comparative genomics of isolates of a Pseudomonas aeruginosa epidemic strain associated with chronic lung infections of cystic fibrosis patients. PLoS ONE, 2014, 9: 1-15

[28] Kalangi SK, Dayakar A, Gangappa D, Sathyavathi R, Maurya RS, Narayana Rao D. Biocompatible silver nanoparticles reduced from Anethum graveolens leaf extract augments the antileishmanial efficacy of miltefosine. Exp Parasitol, 2016, 170: 184-192

[29] Kalishwaralal K, Barathmanikanth S, Ram S, Pandian K, Deepak V, Gurunathan S. Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids Surf B Biointerfaces, 2010, 79: 340-344

[30] Krishna G, Kumar SS, Pranitha V, Alha M, Charaya S. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against Salmonella sp. Int J Pharm Pharm Sci, 2015, 7: 84-88

[31] Kumar A, Singh M, Singh PP, Singh SK, Raj P, Pandey KD. Antioxidant efficacy and curcumin content of turmeric (Curcuma-longa L.) flower. Int J Curr Pharm Rev Res, 2016, 8: 112-114

[32] Lotha R, Shamprasad BR, Sundaramoorthy NS, Ganapathy R, Nagarajan S, Sivasubramanian A. Zero valent silver nanoparticles capped with capsaicinoids containing Capsicum annuum extract, exert potent anti-biofilm effect on food borne pathogen Staphylococcus aureus and curtail planktonic growth on a zebrafish infection model. Microb Pathog, 2018, 124: 291-300

[33] Machado S, Pinto SL, Grosso JP, Nouws HPA, Albergaria JT. Green production of zero-valent iron nanoparticles using tree leaf extracts. Sci Total Environ, 2013, 445–446: 1-8

[34] Masek A, Chrzescijanska E, Latos M, Zaborski M, Podsedek A. Antioxidant and antiradical properties of green tea extract compounds. Int J Electrochem Sci, 2017, 12: 6600-6610

[35] Mehta SK, Chaudhary S, Gradzielski M. Time dependence of nucleation and growth of silver nanoparticles generated by sugar reduction in micellar media. J Colloid Interface Sci, 2010, 343: 447-453

[36] Mittal AK, Kaler A, Banerjee UC. Free radical scavenging and antioxidant activity of silver nanoparticles synthesized from flower extract of Rhododendron dauricum. Nano Biomed Eng, 2012, 4: 118-124

[37] Mittal AK, Kumar S, Banerjee UC. Quercetin and gallic acid mediated synthesis of bimetallic (silver and selenium) nanoparticles and their antitumor and antimicrobial potential. J Colloid Interface Sci, 2014, 431: 194-199

[38] Mühling M, Bradford A, Readman JW, Somerfield PJ, Handy RD. An investigation into the effects of silver nanoparticles on antibiotic resistance of naturally occurring bacteria in an estuarine sediment. Mar Environ Res, 2009, 68: 278-283

[39] Naika HR, Lingaraju K, Manjunath K, Kumar D, Nagaraju G, Suresh D, Nagabhushana H. Green synthesis of CuO nanoparticles using Gloriosa superba L. extract and their antibacterial activity. J Taibah Univ Sci, 2015, 9: 7-12

[40] Nakurte I, Stankus K, Virsis I, Paze A, Rizhikovs J. Characterization of antioxidant activity and total phenolic compound content of birch outer bark extracts using micro plate assay. Environ Technol Resour Proc Int Sci Pract Conf, 2017, 1: 197-201

[41] Neethu S, Midhun SJ, Radhakrishnan EK, Jyothis M. Green synthesized silver nanoparticles by marine endophytic fungus Penicillium polonicum and its antibacterial efficacy against biofilm forming, multidrug-resistant Acinetobacter baumanii. Microb Pathog, 2018, 116: 263-272

[42] Niraimathi KL, Sudha V, Lavanya R, Brindha P. Biosynthesis of silver nanoparticles using Alternanthera sessilis (Linn.) extract and their antimicrobial, antioxidant activities. Colloids Surf B Biointerfaces, 2013, 102: 288-291

[43] Oliver S, Wagh H, Liang Y, Yang S, Boyer C. Enhancing the antimicrobial and antibiofilm effectiveness of silver nanoparticles prepared by green synthesis. J Mater Chem B, 2018, 6: 4124-4138

[44] Oves M, Khan MS, Zaidi A, Ahmed AS, Ahmed F, Ahmad E, Sherwani A, Owais M, Azam A. Antibacterial and cytotoxic efficacy of extracellular silver nanoparticles biofabricated from chromium reducing novel OS4 strain of Stenotrophomonas maltophilia. PLoS ONE, 2013, 8: e59140

[45] Pal S, Ghosh D, Saha C, Chakrabarti AK, Datta SC, Dey SK. Total polyphenol content, antioxidant activity and lipid peroxidation inhibition efficacy of branded tea (Camellia sinensis) available in India. IJTS, 2012, 8: 13-20

[46] Parrino B, Schillaci D, Carnevale I, Giovannetti E, Diana P, Cirrincione G, Cascioferro S. Synthetic small molecules as anti-biofilm agents in the struggle against antibiotic resistance. Eur J Med Chem, 2019, 161: 154-178

[47] Radzig MA, Nadtochenko VA, Koksharova OA, Kiwi J, Lipasova VA, Khmel IA. Antibacterial effects of silver nanoparticles on gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloids Surf B Biointerfaces, 2013, 102: 300-306

[48] Rajasekharreddy P, Rani PU. Biofabrication of Ag nanoparticles using Sterculia foetida L. seed extract and their toxic potential against mosquito vectors and HeLa cancer cells. Mater Sci Eng, C, 2014, 39: 203-212

[49] Ramadan M, Abd-Algader N, El-kamali H, Farrag AH, Ghanem K. Volatile compounds and antioxidant activity of the aromatic herb Anethum graveolens. J Arab Soc Med Res, 2013, 8: 79-88

[50] Ramiréz-Aristizabal LS, Ortiz A, Ospina-Ocampo LF. Evaluation of the antioxidant capacity and characterization of phenolic compounds obtained from tea (Camellia Sinensis) for products of different brands sold in Colombia. Pharmacol Online, 2015, 3: 149-159

[51] Rolim WR, Pelegrino MT, de Araújo Lima B, Ferraz LS, Costa FN, Bernardes JS, Rodigues T, Brocchi M, Seabra AB. Green tea extract mediated biogenic synthesis of silver nanoparticles: characterization, cytotoxicity evaluation and antibacterial activity. Appl Surf Sci, 2019, 463: 66-74

[52] Rolim WR, Pieretti JC, Renó DLS, Lima BA, Nascimento MHM, Ambrosio FN, Lombello CB, Brocchi M, de Souza ACS, Seabra AB. Antimicrobial activity and cytotoxicity to tumor cells of nitric oxide donor and silver nanoparticles containing PVA/PEG films for topical applications. ACS Appl Mater Interfaces, 2019, 11: 6589-6604

[53] Saeb ATM, Alshammari AS, Al-brahim H, Al-rubeaan KA. production of silver nanoparticles with strong and stable antimicrobial activity against highly pathogenic and multidrug resistant bacteria. Sci World J, 2014, 2014: 1-9

[54] San AMM, Thongpraditchote S, Sithisarn P, Gritsanapan W. Total phenolics and total flavonoids contents and hypnotic effect in mice of Ziziphus mauritiana Lam. seed extract. Evidence-Based Complement Altern Med, 2013, 2013: 1-4

[55] Sarsar V, Selwal MK, Selwal KK. Biofabrication, characterization and antibacterial efficacy of extracellular silver nanoparticles using novel fungal strain of Penicillium atramentosum KM. J Saudi Chem Soc, 2015, 19: 682-688

[56] Seabra AB, Manosalva N, De Araujo Lima B, Pelegrino MT, Brocchi M, Rubilar O, Durán N. Antibacterial activity of nitric oxide releasing silver nanoparticles. J Phys: Conf Ser, 2017, 838: 012031

[57] Singh M, Mallick AK, Banerjee M, Kumar R. Loss of outer membrane integrity in gram-negative bacteria by silver nanoparticles loaded with Camellia sinensis leaf phytochemicals: plausible mechanism of bacterial cell disintegration. Bull Mater Sci, 2016, 39: 1871-1878

[58] Singh P, Pandit S, Garnæs J, Tunjic S, Mokkapati VRSS, Sultan A, Thygesen A, Mackevica A, Mateiu RV, Daugaard AE, Baun A, Mijakovic I. Green synthesis of gold and silver nanoparticles from Cannabis sativa (Industrial hemp) and their capacity for biofilm inhibition. Int J Nanomed, 2018, 13: 3571-3591

[59] Smith AW. Biofilms and antibiotic therapy: is there a role for combating bacterial resistance by the use of novel drug delivery systems?. Adv Drug Deliv Rev, 2005, 57: 1539-1550

[60] Sonesson A, Przybyszewska K, Eriksson S, Mörgelin M, Kjellström S, Davies J, Potempa J, Schmidtchen A. Identification of bacterial biofilm and the Staphylococcus aureus derived protease, staphopain, on the skin surface of patients with atopic dermatitis. Sci Rep, 2017, 7: 1-12

[61] Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods, 2000, 40: 175-179

[62] Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet, 2001, 358: 135-138

[63] Sudha A, Jeyakanthan J, Srinivasan P. Green synthesis of silver nanoparticles using Lippia nodiflora aerial extract and evaluation of their antioxidant, antibacterial and cytotoxic effects. Resour Technol, 2017, 3: 506-515

[64] Taylor PK, Yeung ATY, Hancock REW. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol, 2014, 191: 121-130

[65] Vázquez G, Fontenla E, Santos J, Freire MS, González-Álvarez J, Antorrena G. Antioxidant activity and phenolic content of chestnut (Castanea sativa) shell and eucalyptus (Eucalyptus globulus) bark extracts. Ind Crops Prod, 2008, 28: 279-285

[66] Velázquez-velázquez JL, Santos-flores A, Araujo-meléndez J, Sánchez-sánchez R, Velasquillo C, González C, Martínez-castañon G, Martinez-gutierrez F. Anti-biofilm and cytotoxicity activity of impregnated dressings with silver nanoparticles. Mater Sci Eng C, 2015, 49: 604-611

[67] Verma P, Maheshwari SK. Applications of silver nanoparticles in diverse sectors. Int J Nano Dimens, 2019, 10: 18-36

[68] Zayed MF, Eisa WH, Shabaka AA. Malva parviflora extract assisted green synthesis of silver nanoparticles. Spectrochim Acta Part A Mol Biomol Spectrosc, 2012, 98: 423-428

[69] Zhang P, Shao C, Zhang Z, Zhang M, Mu J, Guo Z, Liu Y. In situ assembly of well-dispersed Ag nanoparticles (AgNPs) on electrospun carbon nanofibers (CNFs) for catalytic reduction of 4-nitrophenol. Nanoscale, 2011, 3: 3357-3363

Funding

Fundação de Amparo à Pesquisa do Estado de São Paulo(2018/08194-2)

CONICYT/FONDAP(15130015)

CONICYTE-REDES(180003)