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Molecules 2020, 25, 2023 2 of 14 down the cell wall and several centrifugation and washing steps required for nanoparticle purification. Additionally, extracellular peptides, enzymes, reducing cofactors, and organic materials have significant roles by acting as reducing agents, providing natural capping to synthesize nanoparticles [5]. Crucially, such capping prevents nanoparticle aggregation and helps them to remain stable for long periods of time [2]. The commercial interest in silver nanoparticles lies in their various applications in diverse fields where their potent antimicrobial properties can be harnessed [6]. Recently there has been a drive towards the synthesis of silver nanoparticles by microorganisms [7,8]. In a previous study, our group reported an extracellular cell-free filtrate method for the biological synthesis of silver nanoparticles. The fungal strains were selected based on their silver nanoparticle synthesis capacity, yield of production, resistance to centrifugation and long-term colloidal stability of the obtained nanoparticles following their purification protocols. Moreover, these nanoparticles showed antibacterial activity against Escherichia coli in agar diffusion assays [7]. Another important aspect of the antimicrobial properties of silver nanoparticles is their potential to eradicate or inhibit microbial biofilm formation, which is an important virulence factor in many localized chronic infections [9,10]. One of the most notable emergent biofilm properties is that adhering microorganisms can embed themselves in a self-produced matrix of extracellular polymeric substances (EPS) composed of proteins, polysaccharides, humic acids and DNA. This matrix of EPS acts as the glue that holds together bacterial biofilms, protecting them against host immune systems and environmental challenges, among other exogenous threat to survival and proliferation. Consequently, the polymeric matrix plays a crucial role in antimicrobial resistance by preventing antibiotic penetration inside the biofilm. Despite the EPS-matrix containing water-filled channels required for the exchange of nutrients and metabolic waste-products with their environment, most antimicrobials have difficulty penetrating EPS, either through size limitations or ready adsorption onto the EPS-matrix or to bacterial cell surfaces that can be highly negatively charged at physiological pH, but becoming more positively charged with decreasing pH inside a biofilm. Such phenomena help the survival of internal biofilm cells and illustrate the limitation of traditional molecular approaches to biofilm eradication. In this sense, advances in nanotechnology can provide a great tool [11,12]. For example, reports on silver nanoparticles have shown they are able to diffuse toward the inner part of the biofilm before releasing Ag+ ions, where this penetration leading to a high kill rate against the bacteria in the lower layers of the biofilm [13]. Different nanomaterials, non-adhesive, drug-releasing and contact-killing coatings, are under design to prevent biomaterial-associated infection of implants such as artificial hips and knees. Moreover, nanotechnology is looked at as an extremely promising way to create new antimicrobials and delivery systems, able to penetrate biofilms and kill multidrug resistant strains [14]. Size, shape and surface properties of the resulting nanomaterials are important to consider with respect to the control of biofilm-infection [15]. Nanoparticle size is important for penetration into biofilms [13]; the ideal diameter for NPs in biofilm-infection control would range between five and 100–200 nm, and not exceeding 500 nm [14]. Antimicrobial and antibiofilm mechanisms of silver nanoparticles are not completely known, and they depend on the type of microorganism and the physicochemical properties of the nanoparticle [16,17]. Nanoparticles are able to contact with bacterial cell walls through different interactions, cross microbe membranes, interfere with metabolic pathways, induce changes in membrane shape and function, interact with the microbial cellular machinery to inhibit enzymes, deactivate proteins, induce oxidative stress and electrolyte imbalance, or modify gene expression levels. Given their enormous therapeutic potential, understanding the modes of action responsible for the bactericidal properties of NPs becomes imperative [18]. Furthermore, it is also important to develop accessible, cheap, rapid and reliable methods as alternatives to traditional biochemical methods which often determine only one mechanism of action at sub-cellular level. For this purpose, we used three complementary techniques: transmission electron microscopy (TEM), environmental scanning electronPDF Image | Biofilm Eradication Using Biogenic Silver Nanoparticles
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