Dual Function of Silver Nanoparticles as Matrix Extracell Removal and Antimicrobial Agent in Polymycrobial Biofilms


Mei Shirli Yasinta(1), Hera Lisna Ginawati(2), Nira Ambar Arum(3), Harini Nur Hikmah(4), Sri Sumarsih(5), Mochamad Zakki Fahmi(6), Afaf Baktir(7*)

(1) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(2) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(3) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(4) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(5) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(6) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(7) Department of Chemistry, Airlangga University, Kampus C Mulyorejo, Surabaya 60115, Indonesia
(*) Corresponding Author


Candida albicans often form polymicrobial biofilms along with pathogenic microbes. Silver nanoparticles (AgNPs) were well known to have strong antimicrobial activity. However, their effect on polymicrobial biofilms and the mechanism has never been reported. This study aimed to synthesize AgNPs and study their effects on polymicrobial biofilm represented by C. albicans–E. coli biofilm. Polymicrobial biofilms, formed by clinical isolates of C. albicans and E. coli, were developed from the standardized suspensions of each strain by culturing flat-bottom 96-well microtiter plates for 48 h, then treated with AgNPs. Cell viability was assessed using the tetrazolium salt reduction assay; the extent of biofilm formation was measured by crystal violet staining. AgNPs reduced the polymicrobial biofilm in two ways: by degrading the extracellular matrix and killing both C. albicans and E. coli. The results showed AgNPs is a potential new approach for developing potent anti-biofilms.


silver nanoparticle; polymicrobial biofilm; C. albicans; E. coli; anti-biofilm

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[1] Rabin, N., Zheng, Y., Opoku-Temeng, C., Du, Y., Bonsu, E., and Sintim, H.O., 2015, Biofilm formation mechanisms and targets for developing antibiofilm agents, Future Med. Chem., 7 (4), 493–512.

[2] Gulati, M., and Nobile, C.J., 2016, Candida albicans biofilms: Development, regulation, and molecular mechanisms, Microbes Infect., 18 (5), 310–321.

[3] Burmølle, M., Ren, D., Bjarnsholt, T., and Sørensen, S.J., 2014, Interactions in multispecies biofilms: Do they actually matter?, Trends Microbiol., 22 (2), 84–91.

[4] Nobile, C.J., Johnson, A.D., 2015, Candida albicans biofilms and human disease, Annu. Rev. Microbiol., 69, 71–92.

[5] Bandara, H.M.H.N., Yau, J.Y.Y., Watt, R.M., Jin, L.J., and Samaranayake, L.P., 2009, Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation, J. Med. Microbiol., 58 (12), 1623–1631.

[6] Palanisamy, N.K., Ferina, N., Amirulhusni, A.N., Mohd-Zain, Z., Hussaini, J., Ping, L.J., and Durairaj, R., 2014, Antibiofilm properties of chemically synthesized silver nanoparticles found against Pseudomonas aeruginosa, J. Nanobiotechnol., 12 (1), 2.

[7] Monroe, D., 2007, Looking for chinks in the armor of bacterial biofilms, PLoS Biol., 5 (11), e307.

[8] Peters, B.M., Jabra-Rizk, M.A., O’May, G.A., Costerton, J.W., and Shirtliff, M.E., 2012, Polymicrobial interactions: Impact on pathogenesis and human disease, Clin. Microbiol. Rev., 25 (1), 193–213.

[9] dos Santos, J.D., Piva, E., Vilela, S.F.G., Jorge, A.O.C., and Junqueira, J.C., 2016, Mixed biofilms formed by C. albicans and non-albicans species: A study of microbial interactions, Braz. Oral Res., 30, e23.

[10] Baktir, A., Masfufatun, Hanum, G.R., Amailia, K.R., and Purkan, 2014, Construction and characterization of the intestinal biofilm model of Candida spp, Res. J. Pharm., Biol. Chem. Sci., 5 (1), 204–211.

[11] Harriott, M.M., and Noverr, M.C., 2011, Importance of Candida-bacterial polymicrobial biofilms in disease, Trends Microbiol., 19 (11), 557–563.

[12] Røder, H.L., Sørensen, S.J., and Burmølle, M., 2016, Studying bacterial multispecies biofilms: Where to start?, Trends Microbiol., 24 (6), 503–513.

[13] Fox, E.P., and Nobile, C.J., 2012, A sticky situation: Untangling the transcriptional network controlling biofilm development in Candida albicans, Transcription, 3 (6), 315–22.

[14] Vandecandelaere, I., Matthijs, N., Nelis, H.J., Depuydt, P., and Coenye, T., 2013, The presence of antibiotic-resistant nosocomial pathogens in endotracheal tube biofilms and corresponding surveillance cultures, Pathog. Dis., 69 (2), 142–148.

[15] Samaranayake, Y.H., Bandara, H.M.H.N., Cheung, B.P.K., Yau, J.Y.Y., Yeung, S.K.W., and Samaranayake, L.P., 2014, Enteric gram-negative bacilli suppress Candida biofilms on Foley urinary catheters, APMIS, 122 (1), 47–58.

[16] De Brucker, K., Tan, Y., Vints, K., De Cremer, K., Braem, A., Verstraeten, N., Michiels, J., Vleugels, J., Cammue, B.P.A., and Thevissen, K., 2015, Fungal β-1,3-glucan increases ofloxacin tolerance of Escherichia coli in a polymicrobial E. coli/Candida albicans biofilm, Antimicrob. Agents Chemother., 56 (9), 3052–3058.

[17] Ansari, M.A., Khan, H.M., Khan, A.A., Cameotra, S.S., and Pal, R., 2013, Antibiofilm efficacy of silver nanoparticles against biofilm of extended spectrum β-lactamase isolates of Escherichia coli and Klebsiella pneumoniae, Appl. Nanosci., 4 (7), 859–868.

[18] Panáček, A., Kolář, M., Večeřová, R., Prucek, R., Soukupová, J., Kryštof, V., Hamal, P., Zbořil, R., and Kvítek, L., 2009, Antifungal activity of silver nanoparticles against Candida spp., Biomaterials, 30 (31), 6333–6340.

[19] Li, W.R., Xie, X.B., Shi, Q.S., Zeng, H.Y., Ou-Yang, Y.S., and Chen, Y.B., 2010, Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli, Appl. Microbiol. Biotechnol., 85 (4), 1115–1122.

[20] Abishek, B., and Hemlata, C., 2014, Antibacterial activity of silver nanoparticles conjugated with antibiotics, Bionano Front., 7, 32–35.

[21] McGillicuddy, E., Murray, I., Kavanagh, S., Morrison, L., Fogarty, A., Cormican, M., Dockery, P., Prendergast, M., Rowan, N., and Morris, D., 2017, Silver nanoparticles in the environment: Sources, detection and ecotoxicology, Sci. Total Environ., 575, 231–246.

[22] Manikprabhu, D., and Lingappa, K., 2013, Microwave assisted rapid and green synthesis of silver nanoparticles using a pigment produced by Streptomyces coelicolor klmp33, Bioinorg. Chem. Appl., 2013, 341798.

[23] Blom, M.N., Schooss, D., Stairs, J., and Kappes, M.M., 2006, Experimental structure determination of silver cluster ions (Agn+, 19 ≤ n ≤ 79), J. Chem. Phys., 124 (24), 244308.

[24] Kvitek, L., Panacek, A., Prucek, R., Soukupova, J., Vanickova, M., Kolar, M., and Zboril, R., 2011, Antibacterial activity and toxicity of silver – nanosilver versus ionic silver, J. Phys. Conf. Ser., 304, 012029.

[25] Welch, K., Cai, Y., and Strømme, M., 2012, A method for quantitative determination of biofilm viability, J. Funct. Biomater., 3 (2), 418–431.

[26] Nett, J.E., Cain, M.T., Crawford, K., and Andes, D.R., 2011, Optimizing a Candida biofilm microtiter plate model for measurement of antifungal susceptibility by tetrazolium salt assay, J. Clin. Microbiol., 49, 1426–33.

[27] Ansari, M.A., Khan, H.M., Khan, A.A., Cameotra, S.S., and Alzohairy, M.A., 2015, Anti-biofilm efficacy of silver nanoparticles against MRSA and MRSE isolated from wounds in a tertiary care hospital, Indian J. Med. Microbiol., 33 (1), 101–109.

DOI: https://doi.org/10.22146/ijc.52355

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