Abstract
The aim of the present study was to determine the effect of nisin, 2,3-dihydroxybenzoic acid (DHBA) and a combination of nisin and DHBA incorporated into nanofibers prepared from poly(d,l-lactide) (PDLLA) and poly(ethylene oxide) (PEO) on biofilm formation of a methicillin-resistant strain of Staphylococcus aureus (strain Xen 31). Biofilm formation decreased by 88 % after 24 h of exposure to nanofibers containing nisin and DHBA (NDF), compared to a 63 % decrease when exposed to nanofibers containing only DHBA (DF) and a 3 % decrease when exposed to nanofibers containing only nisin (NF). Planktonic cell numbers of biofilms exposed to nanofibers without nisin or DHBA (CF) and NF increased from no detectable OD595nm readings to 0.35 and 0.3, respectively, within the first 8 h of exposure, followed by a steady decline over the following 16 h. Planktonic cells of biofilms treated with DF increased from no detectable OD595nm readings to 0.05 after 8 h of exposure and remained more-or-less constant for the duration of the experiment. Planktonic cells of biofilms exposed to NDF increased from OD595nm 0.03 after 8 h of exposure and to 0.2 over the following 16 h. Biofilm formation increased with increasing concentrations of FeCl3·6H2O, which suggests that iron is required for S. aureus Xen 31 to form a biofilm. However, when exposed to NDF, biofilm formation decreased significantly in the presence of increasing concentrations of iron. This suggests that NDF may be used to prevent biofilm formation of MRSA and control infection.
Similar content being viewed by others
References
Abriouel H, Valdivia E, Gálvez A, Maqueda M (1998) Response of Salmonella choleraesuis LT2 spheroplasts and permeabilized cells to the bacteriocin AS-48. Appl Environ Microbiol 11:4623–4626
Ahire JJ, Neppalli R, Heunis TDJ, Van Reenen AJ, Dicks LMT (2014) 2,3-Dihydroxybenzoic acid electrospun into poly(d,l lactide) (PDLLA)/poly(ethylene oxide) (PEO) nanofibers inhibited the growth of Gram-positive and Gram-negative bacteria. Curr Microbiol (in press). doi: 10.1007/s00284-014-0635-3
Ahire JJ, Dicks LMT (2014) 2,3-Dihydroxybenzoic acid-containing nanofiber wound dressings inhibits biofilm formation by Pseudomonas aeruginosa. Antimicrob Agents Chemother 58(4):2098–2104
Ardehali R, Shi L, Janatova J, Mohammad SF, Burns GL (2002) The effect of apo-transferrin on bacterial adhesion to biomaterials. Artif Organs 26:512–520
Bauer R, Dicks LMT (2005) Mode of action of lipid II-targeting lantibiotics. Int J Food Microbiol 101:201–216
Bizani D, Motta AS, Morrissy JAC, Terra RMS, Souto AA, Brandelli A (2005) Antibacterial activity of cerein 8A, a bacteriocin-like peptide produced by Bacillus cereus. Int Microbiol 8:125–131
Blatt J, Taylor SR, Kontoghiorghes GJ (1989) Comparison of activity of deferoxamine with that of oral iron chelators against human neuroblastoma cell lines. Cancer Res 49:2925–2927
Bullen JJ, Rogers HJ, Spalding PB, Ward CG (2005) Iron and infection: the heart of the matter. FEMS Immunol Med Microbiol 43:325–330
Bullen JJ, Rogers HJ, Spalding PB, Ward CG (2006) Natural resistance, iron and infection: a challenge for clinical medicine. J Med Microbiol 55:251–258
Burns JL, Mancoll JS, Phillips LG (2003) Impairments to wound healing. Clin Plast Surg 30:47–56
Chatterjee SS, Otto M (2013) Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves. Clin Epidemiol 5:205–217
Cui B, Smooker PM, Rouch DA, Daley AJ, Deightona MA (2013) Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J Clin Microbiol 51:9–14
Delves-Broughton J (1993) The use of EDTA to enhance the efficacy of nisin towards gram-negative bacteria. Int Biodeterior Biodegrad 32:87–97
Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
Hancock RE, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24:1551–1557
Heunis TDJ, Bshena O, Klumperman B, Dicks LMT (2011) Release of bacteriocins from nanofibers prepared with combinations of poly(d,l-lactide) (PDLLA) and poly(ethylene oxide) (PEO). Int J Mol Sci 12:2158–2173
Heunis TD, Smith C, Dicks LMT (2013) Evaluation of a nisin-eluting nanofiber scaffold to treat Staphylococcus aureus-induced skin infections in mice. Antimicrob Agents Chemother 57:3928–3935
Huang T, Long M, Huo B (2010) Competitive binding to cuprous ions of protein and BCA in the bicichoninic acid protein assay. Open Biomed Eng J 4:271–278
Johnson M, Cockayne A, Morrissey JA (2008) Iron-regulated biofilm formation in Staphylococcus aureus Newman requires ica and the secreted protein Emp. Infect Immun 76:1756–1765
Kopermsub P, Mayen V, Warin C (2011) Potential use of niosomes for encapsulation of nisin and EDTA and their antibacterial activity enhancement. Food Res Int 44:605–612
Kopermsub P, Mayen V, Warin C (2012) Nanoencapsulation of nisin and ethylene diamine tetra acetic acid in niosomes and their antimicrobial activity. J Sci Res 4:457–465
Lin MH, Shu JC, Huang HY, Cheng YC (2012) Involvement of iron in biofilm formation by Staphylococcus aureus. PLoS One 7(3):e34388:1–e34388:7
Lipsky BA, Berendt AR, Deery HG, Embil JM, Joseph WS, Karchmer AW, LeFrock JL, Lew DP, Mader JT, Norden C, Tan JS (2006) Diagnosis and treatment of diabetic foot infections. Plast Reconstr Surg 117:212S–238S
Liu H, Ding X, Zhou G, Li P, Wei X, Fan Y (2013) Electrospinning of nanofibers for tissue engineering applications. J Nanomater 2013:1–11
Mataraci E, Dosler S (2012) In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin-resistant Staphylococcus aureus biofilms. Antimicrob Agents Chemother 56:6366–6371
Mey AR, Craig SA, Payne SM (2005) Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. Infect Immun 73:5706–5719
Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207–228
O’Toole GA (2011) Microtiter dish biofilm formation assay. J Vis Exp 47:1–2
Payne SM (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235:329–344
Rodriguez JM (1996) Antimicrobial spectrum, structure, properties and mode of action of nisin, a bacteriocin produced by Lactococcus lactis. Int J Food Sci Technol 2:61–68
Sapan CV, Lundblad RL, Price NC (1999) Review: colorimetric protein assay techniques. Biotechnol Appl Biochem 29:99–108
Schved F, Henis Y, Juven BJ (1994) Response of spheroplasts and chelator-permeabilized cells of Gram-negative bacteria to the action of the bacteriocins pediocin SJ-1 and nisin. Int J Food Microbiol 21:305–314
Severina E, Severin A, Tomasz A (1998) Antibacterial efficacy of nisin against multidrug-resistant Gram-positive pathogens. J Antimicrob Chemother 41:341–347
Singh AP, Prabha V, Rishi P (2013) Value addition in the efficacy of conventional antibiotics by nisin against Salmonella. PLoS One 8(10):e76844
Sousa M, Ousingsawat J, Seitz R, Puntheeranurak S, Regalado A et al (2007) An extract from the medicinal plant Phyllanthus acidus and its isolated compounds induce airway chloride secretion: a potential treatment for cystic fibrosis. Mol Pharmacol 71:366
Stevens KA, Sheldon BW, Klapes NA, Klaenhammer TR (1991) Nisin treatment for inactivation of Salmonella species and other Gram-negative bacteria. Appl Environ Microbiol 57:3613–3615
Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113
Sudagidan M, Yemenicioğlu A (2012) Effects of nisin and lysozyme on growth inhibition and biofilm formation capacity of Staphylococcus aureus strains isolated from raw milk and cheese samples. J Food Prot 9:1627–1633
Tan S, Huang X, Wu B (2007) Some fascinating phenomena in electrospinning processes and applications of electrospun nanofibers. Polym Int 56:1330–1339
Wenk J, Foitzik A, Achterberg V, Sabiwalsky A, Dissemond J et al (2001) Selective pickup of increased iron by deferoxamine-coupled cellulose abrogates the iron-driven induction of matrix-degrading metalloproteinase 1 and lipid peroxidation in human dermal fibroblasts in vitro: a new dressing concept. J Invest Dermatol 116:833–839
Wu Y, Outten FW (2009) IscR controls iron-dependent biofilm formation in Escherichia coli by regulating type I fimbria expression. J Bacteriol 191:1248–1257
Yao S, Wang X, Liu X, Wang R, Deng C, Cuil F (2013) Effects of ambient relative humidity and solvent properties on the electrospinning of pure hyaluronic acid nanofibers. J Nanosci Nanotechnol 13:4752–4758
Acknowledgments
Ahire JJ is grateful to the Claude Leon Foundation, Cape Town, South Africa, for a postdoctoral fellowship.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ahire, J.J., Dicks, L.M.T. Nisin Incorporated With 2,3-Dihydroxybenzoic Acid in Nanofibers Inhibits Biofilm Formation by a Methicillin-Resistant Strain of Staphylococcus aureus . Probiotics & Antimicro. Prot. 7, 52–59 (2015). https://doi.org/10.1007/s12602-014-9171-5
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-014-9171-5