Role of Silver Ions in Destabilization of Intermolecular Adhesion Forces Measured by Atomic Force Microscopy in Staphylococcus epidermidis Biofilms

Abstract

In this paper, we report on the potential use of atomic force microscopy (AFM) as a tool to measure the intermolecular forces in biofilm structures and to study the effect of silver ions on sessile Staphylococcus epidermidis cell viability and stability. We propose a strategy of destabilizing the biofilm matrix by reducing the intermolecular forces within the extracellular polymeric substances (EPSs) using a low concentration (50 ppb) of silver ions. Our AFM studies on the intermolecular forces within the EPSs of S. epidermidis RP62A and S. epidermidis 1457 biofilms suggest that the silver ions can destabilize the biofilm matrix by binding to electron donor groups of the biological molecules. This leads to reductions in the number of binding sites for hydrogen bonds and electrostatic and hydrophobic interactions and, hence, the destabilization of the biofilm structure.Microorganisms attach to living and nonliving surfaces, including those of indwelling medical devices and potable water system piping, and form biofilms that consist of extracellular polymers. Biofilms are the source of free-floating bacteria in drinking water, which poses a health risk (5). In biomedical areas, biofilms are a common source of medical device-related infections, such as acute bacterial infection of dental plaque (33), catheter-related bloodstream infection (7, 9, 34), and heart valves endocarditis (22). Although antibiotics like vancomycin and tobramycin (8, 23) are used to treat these infections, most of these infections persist. The use of antimicrobial agents and antibiotics for the treatment of these infections is limited, as the biofilms create an environment that enhances antimicrobial resistance (3,16,19). In general, the most important contribution of biofilms' antimicrobial resistance can be related to the properties of extracellular polymeric substances (EPSs), such as diffusion, sorption, water binding, mass transport, and mechanical stability. The EPSs of biofilms contain considerable amounts of polysaccharides, proteins, nucleic acids, and lipid (30), which are responsible for maintaining the structural integrity of the biofilm and providing an ideal matrix for bacterial cell growth (15). Intermolecular interactions between the various functional groups within these macromolecules serve to strengthen the overall mechanical stability of the EPSs and, hence, the survivability of the enclosed microorganisms.It is reported that when silver ions bind to biological molecules containing thio, amino, carboxylate, imidazole, or phosphate groups, they inhibit activities that are vital to the bacteria's regulatory processes and cause bacterial inactivation (26,27). Silver ions also act by displacing other essential metal ions, such as Ca 2ϩ and Zn 2ϩ . Silver cations exhibit broad antimicrobial action at low concentrations, and they are already being used for the treatment of burn wounds (24) and traumatic injuries (6). Silver ions also display low levels of toxicity to humans (1) and are safe agents for the removal of biofilms. B...

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“…Researchers have been able to show that the EPS is mainly made up of polysaccharides (~24.5%) and proteins (~82.8%), polysaccharides existing in nature either as neutral or as polyanionic, as in the case for the EPS of Gram-negative bacteria 6,17,20,28,34,45 . The EPS also contains teichoic acid (secondary cell wall polymers), nucleic acids, phospholipids and other polymeric substances 7,8 . Intermolecular interactions between the various functional groups within the EPS macromolecules serve to strengthen the overall mechanical stability of the EPS and, hence the survival of the enclosed microorganisms 7 .…”

“…The EPS also contains teichoic acid (secondary cell wall polymers), nucleic acids, phospholipids and other polymeric substances 7,8 . Intermolecular interactions between the various functional groups within the EPS macromolecules serve to strengthen the overall mechanical stability of the EPS and, hence the survival of the enclosed microorganisms 7 .…”