Introduction

Metallic nanoparticles (NPs) have drawn a lot of attention, due to their unique characteristics and their promising applications in optical, electrical, mechanical, chemical and medical fields. They also have the ability to behave as antiviral agents [1 – 3]. Knowledge of the toxicity of NPs to human health is not fully complete but NPs are considered toxic and are classified into four different categories: (i) Nanomaterials based on metallodendrimers. Metallodendrimers composed of nanosized metals and are conjugated with organic polymers are typically used in molecular electronics and catalysis [4, 5]. (ii) Carbon-based nanomaterials made of carbon nanotubes or fullerenes. Such accumulate in living cells causing cytotoxicity and pulmonary toxicity [6 – 9]. (iii) Metal based nanomaterials, including quantum dots and various metallic NPs such as Ag, Au, and Pt NPs and Metal oxides, such as Al₂O₃, CrO₃, Fe₃O₄, SiO₂, TiO₂ and ZnO₂. Such metal oxides have been found to reason adverse effects causing conditions such as oxidative stress, inflammation of endothelial cells, apoptosis and ecotoxicity [10 – 13]. (iv) Metal NPs composites that combine a few different NPs to form bulk-type materials such as Fe-Pt NPs. Such composites have the power to cause mutagenicity in cells like bacterial cells [14].

Properties of NPs

The chemical and physical properties of NPs differ greatly from those of their corresponding bulk. Their sizes can range within the nanoscale up to 100 nm.

Nanomaterials have been found to have many different shapes and structures. They can exist as spheres, plates, tubes, needles, sheets, etc. Their distinct sizes and shapes contribute to their toxicity, for instance, single-wall nanotubes are more toxic than multi-wall nanotubes [15, 16]. In order to characterise NPs, it is important to fully understand their physicochemical properties; (a) size distribution, (b) shape, (c) structure, (d) their nature to agglomerate/aggregate, (e) surface area, (f) surface charge, (g) surface chemistry and (h) porosity [17]. Many methods have been employed to investigate these properties, including the uses of scanning and transmission electron microscopes (SEM & TEM), X-ray diffraction, zeta potential, spectroscopic techniques (i.e. UV, IR, etc.), isothermal absorption and dynamic light scattering (DLS) [17].

Figure 1: a An SEM image of colloidal gold nanoparticles. b) A TEM image of a single gold nanoparticle.   Click here to View figure

Some nanoparticles rely on illumination or on the application of a magnetic field to generate heat [18]. For example, light-absorbing gold nanoparticles can be attached to bacteria, which allows the use of lasers to target the bacteria to be killed [19].

If a system lacks certain conditions, then the NPs may aggregate and form their corresponding bulk. They tend to aggregate by fusion and deposition. NPs in gases usually agglomerate faster than they do when in liquid. They form primary agglomerates as primary free NPs stick to each other via interparticle interactions such as weak van der Waals, electrostatic and sintered bonds [20]. Particle-particle interactions that govern the nanoscale are van der Waals, stronger polar and covalent or electrostatic interactions. Viscosity and polarisability of the aqueous environment also influence these interactions in order to form agglomerates. Attractive and repulsive forces determine the states of individual and collective NPs.

Many of today’s NPs are modified chemically or are engineered by surface modification that will hence avoid agglomeration. In the presence of certain chemical agents, surfaces of NPs are allowed to become greatly modified so that they are indirectly stabilised against coagulation [17, 21].

Demonstration of Potential Hazard to Bacteria

Currently addressed concerns are related to human cells or health. However, impacts of NPs that exist on other living organisms are important for discussion, such as those on prokaryotes like bacteria and many other unicellular microorganisms. Unicellular microorganisms can be used as models for testing NP-toxicity analysis, for they are more sensitive than human fibroblast [22, 23].

Studies have been performed on isolated cultures and not on microbial communities that can exhibit more complex and antagonistic interactions. Some substances have been established already as being antimicrobial agents, such as TiO₂ nanoparticles that work by inhibiting fouling processes by E. coli when the system is placed under UV illumination [24].

NPS enter microorganisms in their food, and become parts of their food chain. This, eventually, leads to the disrupting of the ecological balance, causing cellular toxicities at certain levels.  Entry of NPs into these microorganisms takes place via various means, of which include physical rupturing of cell membrane, wall or endocytosis. It has been reported that metallic NPs have the ability of either passing through to the cell cytoplasm or remain attached to the cell surface membrane [25, 26].

Bacterial cells can also undergo lysis if their cell walls are damaged. Research has demonstrated that metal NPs are capable of damaging bacterial cell walls as they release ions. This causes increased membrane permeability, loss of the proton motive force and efflux of intracellular components [27]. Nanoparticles first attach and anchor the surface of bacterial cell walls. Large numbers of electrostatic forces and molecular interactions are involved at this first stage of interaction [28, 29]. Damages caused at this stage include structural and morphological changes. Any damages can also result in cell death [29, 30].

Nanoparticles tend to associate with enzymes, membrane porins, chaperones or periplasmic peptide-binding proteins of bacterial cell wall. And damage can lead to alterations and eventually affect bacterial enzymatic activities. This may result in morphological changes such as filamentation and DNA coagulation [28].

Different toxicities of NPs are exhibited, which are dependent on two main aspects: (i) the nature of NPs, including their size, morphology and chemical properties. (ii) NPs’ different interactions with different microbial species. The activities are also dependent on the type of bacterial organisms and can be highly related to their cell wall structures and their outer membrane arrangements. This is because significant differences exist between gram-positive bacteria and gram-negative bacteria. Outer membranes and unique periplasmic spaces are exhibited by gram-negative bacteria but not by gram-positive bacteria [28, 31].

Disaggregation of the exopolysaccharide matrix, cell separation, elongation and formation of small clusters are produced at NPs first interaction with the bacterial cell walls.

The disruption of cell membrane becomes more predominant at the second phase of interaction between NPs and bacterial cell walls. The cell wall perforates and thickens [32].

Figure 2: a schematic representation of a contracted cell with intracellular material being released.   Click here to View figure

Toxicity assays of NPs using bacteria as models

Microorganisms exist in almost every environment available on earth. Their flexibility and adaptability allows them to survive under extreme conditions such as anaerobic, high heat conditions. As a whole, they produce the majority of the biomass in aquatic systems. Plants are the primary biomass in terrestrial systems, but their survival, however, is dependent on the activity of microorganisms for the breakdown of dead matter and hence the recycling of needed nutrients. Microorganisms play a major part in the cycling of carbon, phosphorus, nitrogen and other useful minerals. Microorganisms are also essential components of soil health and have the features that will allow them to serve as potential mediators of transformations. These will affect nanoparticle mobility and toxicity in the external and internal environment. Evaluation of microbial toxicity allows extrapolation of the observed effects of chemicals on microorganisms to other higher level organisms in the food chain/web.

For convenience, the Quantitative Structure Activity Relationships (QSARs) method is used to calculate any impact on other organisms based on chemical structure. This method joins mathematical relationships between the structure of chemicals and their likelihood to increase the toxicity of compounds. A numerical value is assigned to each chemical and the sum of its compound gives the overall toxicity. Similar calculations can also be used to extrapolate the toxicity of a chemical to an organism based on its toxicity to an unrelated organism [33].

To investigate the detrimental effects of NPs on different organisms along with their impacts and mode of action, specific microorganisms can be used in toxicity assays. It has been reported that there are two major effects of NPs on bacteria. NPs are able to encourage oxidative toxicity in addition to damaging the cell membranes of many if not all cells. Currently, however, modes of action of these NPs in bacterial cells are not yet fully understood.

Assessing toxicity of NPs using bacteria as the target cell is very helpful in allowing the understanding of many of the concepts involved. Bacterial assays are faster, cheaper, more sensitive, and are easily handled compared to, for example, mammalian cells. Different NPs all possess different toxicity levels and they are all dependant on many of the morphological features associated with the difference in involved atoms. Therefore, they will all have different effects on living cells. Likewise, they will all have different effects on different cells [34]. It is just that today’s knowledge on the toxicity of NPs is insufficient to allow the identification of any systematic rules that govern the toxicological properties of all the products of nanotechnology [35].

The biocidal effectiveness of metal nanoparticles has also been suggested to be a result of both their size and their high surface-to0-volume ratio. These characteristics allow the NPs to interact with bacterial membranes [36].

Mechanism of Action

The mechanisms by which nanoparticles work by are not yet fully understood, however, there are three proposed mechanisms that are widely accepted today. (1) Cells uptake metal ions causing depletion of intracellular ATP production and disruption of DNA replication [37]. (2) Reactive oxygen species generated from metal NPs and metal ions followed by oxidative damage to cellular structures [31] as shown in figure 3. (3) The accumulation and dissolution of metal NPs in the bacterial membranes leading to the permeability changes and the dissipation of the proton motive force [38, 39].

Figure 3: A schematic representation of gram negative and gram positive bacteria being attacked by ROS produced from nanoparticles using UV irradiation which in turn breaks the protective coating allowing the nanoparticles to enter the bacterial cells.   Click here to View figure

Silver nanoparticles: Silver nanoparticles cause envelope protein precursors to accumulate and the proton motive force to dissipate. Silver nanoparticles work by destabilising the outer membrane, cause the potential of the plasma membrane to fall rapidly and cause the levels of intracellular ATP to decrease [37].Silver nanoparticles are revealed to accumulate in the cell membranes and some penetrated into the cells [40].

Figure 4: a A TEM image of TiO2 nanoparticles. b) E.coli ATCC 10536 growing on the LB broth after 4h with TiO2 nano-particles.   Click here to View figure

Gold nanoparticles: Gold nanoparticles are biocompatible and are exploited in organisms [41, 42]. Nanomaterials based on gold, such as gold nanorods, gold nanoshperes and gold nanocages, have the capability of destroying cancer cells and bacteria via chemotherapy [43, 44]. Antibacterial activities of gold nanoparticles can be enhanced by adding antibiotics [45].

Magnesium oxide nanoparticles are usually prepared through an aerogel procedure producing what is known to be AP-MgO with square and polyhedral shaped nanoparticles of diameters of around 4nm [46]. One of their key properties is their ability to adsorb and retain for a long time huge amounts of elemental chlorine and bromine [47]. AP-MgO also exhibits biocidal activity against some gram-negative bacteria and spores. Their high surface area and enhanced surface reactivity allows the magnesium oxide nanocrystals to adsorb and carry a significant amount of active halogens. Many particles are allowed to cover the bacteria cells to a high extent because of their extremely small sizes. This allows them to bring the halogens to an active form [48].

Zinc oxide nanoparticles have been found to be very toxic. They are stable under harsh processing conditions and have potent antimicrobial properties [49]. Some studies have shown that zinc oxide nanoparticles have selective toxicity to bacteria and minimal effect on human cells [50 – 53]. They have been reported to inhibit the growth of certain bacteria by disintegrating the cell membrane and increasing the membrane permeability [54]. It has also been reported that the hydrogen peroxide generated from the surface of the zinc oxide is an effective means for the growth inhibition of bacteria [55]. In other studies, zinc oxide nanoparticles have been found to release Zn²⁺ ions that damage the cell membrane and interact with intracellular contents [50].

TiO₂ particles are catalysts that can catalyse the killing of bacteria using UV light at wavelengths of less than 385 nm [56 – 58]. Photo-excited TiO₂ particles can generate active free hydroxyl radicals, leading to the antimicrobial effect of TiO₂[59 – 61].  Nanostructured TiO₂ on UV radiation can be used as an effective means for reducing infection time by eliminating pathogens on food surfaces [56].

Copper oxide nanoparticles are not fully investigated to give sufficient information on their antimicrobial effects, however, copper oxide is cheaper than silver and finds a wide application [62]. They have extremely large surface area and unusual crystal morphologies as a result of how they are prepared and so find potential application as antimicrobials [49]. However, high concentrations of copper oxide nanoparticles are needed to achieve bactericidal effects [63].

Aluminium nanoparticles carry a positive charge on its surface at near-neutral pH. Electrostatic attraction is produced between the positive alumina nanoparticles and the negative E. coli cells, causing the particles to adhere to the cells on the bacterial surfaces [64]. Adhesion increases with nanoparticle concentration. With this, there was a negative correlation between bacterial growths against nanoparticle concentration [65]. Antimicrobial activity of the alumina oxide is attributed to the production of reactive oxygen species (ROS), that causes the disruption of cell walls and consequently cell death [66].

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