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Nanomaterials 2020, 10, 376 14 of 22 basal planes of GO, membrane stress of bacteria can be induced, resulting in disruption and physical damage to cell membranes. The sharp edges of graphene sheets act as nanoknives, cutting the bacterial cell membrane, which leads to the leakage of intracellular components followed by cell death [59]. Wrapping and trapping of bacterial membranes by the flexible thin sheets of GO after their direct contact has also been proposed as another antimicrobial mechanism of the graphene materials [54,55,60]. In this scenario, bacterial cells die by being isolated from the growth medium. Oxidative stress is considered a predominant mechanism of bacterial inactivation of GO [59,61]. In bacterial cells exposed to GO, oxidative interactions play a key role due to the oxidation capacity of graphene material. Oxidative stress can occur through either a reactive oxygen species (ROS)-dependent or a ROS-independent pathway. In the first case, oxidative stress is mediated by the production of ROS, which can damage cellular components. In the second one, however, the production of ROS is not involved, being the charge transfer from the cellular membrane to graphene surface that induces cell death. Ruiz et al. [50] investigated the effect of colloidal GO on bacterial (E. coli) growth in Luria–Bertani (LB) nutrient broth, observing a dramatic increase in microbial cell proliferation. The microbial assays showed the precipitation of GO in the culture media when bacteria were present. The scanning electron microscopy (SEM) analysis of this precipitate revealed that it was formed by a thick bacterial biofilm containing a large mass of aggregated cells and extracellular polymeric material. The authors suggested that the GO precipitates acted as scaffolds for cell surface attachment, proliferation, and biofilm formation. Chen et al. [51] also found the formation of anaerobic membrane scaffolds by GO suspensions in bacterial growth medium, which facilitated proliferation of gut microbiota. Hui et al. [62] studied the antimicrobial properties of GO in saline and LB broth. The results showed that LB broth made GO inactive, observing an increase in bacterial growth. The loss of antibacterial activity was attributed to the noncovalent adsorption of LB components on GO basal planes. From the above-mentioned studies, it has been inferred that the culture medium plays a key role in the toxicity of GO against bacteria. More recently, Gusev et al. [63], in their study of the interaction of E. coli with reduced graphene oxide (rGO), also demonstrated the important role of the culture medium in the antimicrobial properties of rGO. Regarding the GO–AgNP-A sample, MIC/2, MIC, and MICx2 were the nanomaterial concentrations analyzed for each microorganism. The results obtained are presented in Figure 7, where it can be observed that microbial growth was completely prevented at one of the concentrations for all the microorganisms. The curves show four distinct growth phases, lag, log, stationary, and death phases. The lag phase corresponds to the delay before exponential growth begins. In the log or exponential phase, cell division proceeds at a constant rate, whereas in the stationary phase, the conditions become unfavorable for growth and microbes stop replicating and reach an equilibrium level. Finally, in the death phase, cells lose viability. The length of the lag phase is the time that it takes for the different inoculums before an increase in cell number is observed. When microorganisms are cultivated in fresh medium and have to face environmental changes, they enter the lag phase, during which cell growth stops. This allows the cells to adapt to the new situation and to synthesize the cellular components necessary for growth. Depending on the cell structure, the type of antimicrobial agent and its concentration, the growth profile differs [64]. According to Table 3, the MIC value for C. albicans was 32 μg/mL, and this can also be confirmed in the growth curves (Figure 7a) where the yeast growth was inhibited for 24 h at this concentration. However, 64 μg/mL of GO–AgNP-A was required to fully inhibit the growth of C. albicans after 50 h of incubation with the nanomaterial. For S. aureus, the concentration causing at least 50% growth inhibition was also 32 μg/mL, although after 35 h, the inhibitory effect disappeared (Figure 7b), and 64 μg/mL of GO–AgNP-A inhibited the growth of S. aureus until 60 h. On the other hand, the two Gram-negative bacteria had an MIC value of 64 μg/mL. However, the antibacterial effect of this concentration on P. aeruginosa ceased after 32 h, while with respect to E. coli, the antibacterial effect was stable over time (Figure 7c,d). In view of all the results, it could be concluded that the GO–AgNP-A nanohybrid exhibited dose- and time-dependent antimicrobial activity. The concentration of GO–AgNP-A thatPDF Image | Graphene Oxide–Silver Nanoparticle Nanohybrids
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