IntechOpen

Home > Books > Antimicrobial Resistance - A One Health Perspective

Open access peer-reviewed chapter

Antimicrobial Effect of Titanium Dioxide Nanoparticles

Written By

Carol López de Dicastillo, Matias Guerrero Correa, Fernanda B. Martínez, Camilo Streitt and Maria José Galotto

Submitted: 31 August 2019 Reviewed: 18 December 2019 Published: 27 January 2020

DOI: 10.5772/intechopen.90891

Antimicrobial Resistance IntechOpen
Antimicrobial Resistance A One Health Perspective Edited by Mihai Mares, Swee Hua Erin Lim and Kok-Song Lai

From the Edited Volume

Antimicrobial Resistance - A One Health Perspective

Edited by Mihai Mareș, Swee Hua Erin Lim, Kok-Song Lai and Romeo-Teodor Cristina

Book Details Order Print

Chapter metrics overview

2,855 Chapter Downloads

View Full Metrics
Advertisement

Abstract

The widespread use of antibiotics has led to the emergence of multidrug-resistant bacterial strains, and therefore a current concern for food safety and human health. The interest for new antimicrobial substances has been focused toward metal oxide nanoparticles. Specifically, titanium dioxide (TiO2) has been considered as an attractive antimicrobial compound due to its photocatalytic nature and because it is a chemically stable, non-toxic, inexpensive, and Generally Recognized as Safe (GRAS) substance. Several studies have revealed this metal oxide demonstrates excellent antifungal and antibacterial properties against a broad range of both Gram-positive and Gram-negative bacteria. These properties were significantly improved by titanium dioxide nanoparticles (TiO2 NPs) synthesis. In this chapter, latest developments on routes of synthesis of TiO2 NPs and antimicrobial activity of these nanostructures are presented. Furthermore, TiO2 NPs favor the inactivation of microorganisms due to their strong oxidizing power by free radical generation, such as hydroxyl and superoxide anion radicals, showing reductions growth against several microorganisms, such as Escherichia coli and Staphylococcus aureus. Understanding the main mechanisms of antimicrobial action of these nanoparticles was the second main purpose of this chapter.

Keywords

  • titanium dioxide
  • nanoparticles
  • green synthesis
  • antimicrobial activity

1. Introduction

The incidence of microbial attack in different sectors such as food, textiles, medicine, water disinfection, and food packaging leads to a constant trend in the search for new antimicrobial substances. The increased resistance of some bacteria to some antibiotics and the toxicity to the human body of some organic antimicrobial substances has increased the interest in the development of inorganic antimicrobial substances. Among these compounds, metal and metal oxide compounds have attracted significant attention due to their broad-spectrum antibacterial activities. On the other hand, nanoscale materials are well known thanks to their increased properties due to their high surface area-to-volume ratio. Antimicrobial NPs have shown excellent and different activities from their bulk properties [1, 2].

During last decades, metal oxide nanoparticles, such as zinc oxide (ZnO), manganese oxide (MgO), titanium dioxide (TiO2), and iron oxide (Fe2O3), have been extensively applicable thanks to their unique physiochemical properties in biological applications. Among metal oxide antimicrobial agents, TiO2 is a valuable semiconducting transition metal oxide material and shows special features, such as easy control, reduced cost, non-toxicity, and good resistance to chemical erosion, that allow its application in optics, solar cells, chemical sensors, electronics, antibacterial and antifungal agents [3]. In general, TiO2 nanoparticles (TiO2 NPs) present large surface area, excellent surface morphology, and non-toxicity in nature. Several authors have reported that TiO2 NPs have been one of the most studied NPs thanks to their photocatalytic antimicrobial activity, exerting excellent bio-related activity against bacterial contamination [4, 5, 6, 7].

Antimicrobial activity of nanoparticles is highly influenced by several intrinsic factors such as their morphology, size, chemistry, source, and nanostructure [8, 9, 10, 11]. Specifically, antimicrobial activity of TiO2 NPs is greatly dependent on photocatalytic performance of TiO2, which depends strongly on its morphological, structural, and textural properties [12]. Several TiO2 NPs have been developed through different methods of synthesis. Specifically, in this chapter, eco-friendly synthesis based on biological sources, such as natural plant extracts and metabolites from microorganisms, which have resulted in TiO2 NPs with different size, shape, morphology, and crystalline structures will be presented. Titanium dioxide produces amorphous and crystalline forms and primarily can occur in three crystalline polymorphous: anatase, rutile, and brookite. Studies on synthesis have stated that the crystalline structure and morphology of TiO2 NPs is influenced by process parameters such as hydrothermal temperatures, starting concentration of acids, etc. [13]. The crystal structures and the shape of TiO2 NPs are both the most important properties that affect their physicochemical properties, and therefore their antimicrobial properties [14]. Regarding the crystal structures, anatase presents the highest photocatalytic and antimicrobial activity. Some works have shown that anatase structure can produce OH˙ radicals in a photocatalytic reaction, and as it will be clearly explained below, bacteria wall and membranes can be deadly affected [15, 16].

Advertisement

2. Antimicrobial activity of titanium dioxide NPs

2.1 Latest tendencies on TiO2 nanoparticle synthesis

The potential health impact and toxicity to the environment of NPs is currently an important matter to be addressed. Several works have confirmed that metal oxide NPs conventionally synthesized using chemical methods, such as sol–gel synthesis and chemical vapor deposition, have shown different levels of toxicity to test organisms [17, 18, 19, 20]. In recent years, researchers have emphasized on the development of nanoparticles promoted through environmental sustainability and processes characterized by an ecological view, mild reaction conditions, and non-toxic precursors. Due to this growing sensitivity toward green chemistry and biological processes, ecological processes are currently being investigated for the synthesis of non-toxic nanoparticles.

These biological methods are considered safe, cost-effective, biocompatible, non-toxic, sustainable, and environmentally friendly processes [20]. Furthermore, it has been described that chemically synthesized NPs have exhibited less stability and added agglomeration, resulting in biologically synthesized NPs that are more dispersible, stable in size, and the processes consuming less energy [21].

These biosynthetic methods, also called “green synthesis,” use various biological resources available in nature, including live plant [22], plant products, plant extracts, algae, fungi, yeasts [23], bacteria [24], and virus for the synthesis of NPs. Among these methods, the processes that use plant-based materials are considered the most suitable for large-scale green synthesis of NPs with respect to their ease and safety [25]. On the other hand, the reduction rate of metal ions in the presence of the plant extract is much faster compared to microorganisms, and provides stable particles [26]. Plants contain biomolecules that have been highly studied by researchers like phenols, nitrogen compounds, terpenoids, and other metabolites. It is well known that the hydroxyl and carboxylic groups present in these biocompounds act as stabilizers and reducing agents due to their high antioxidant activity [12]. Thus, plant extracts have been studied as one of the best green alternatives for metal oxide nanoparticles synthesis [27]. In recent years, TiO2 nanoparticles have been obtained by using different plant extracts, but not all of them have been studied for their antimicrobial activity. Table 1 presents a compilation of synthesized TiO2 nanoparticles from green synthesis by using plant extracts that were tested against different microorganisms.

Source Titanium precursor Size (nm) Shape/crystal structure Target microorganism (method)
Azadirachta indica leaves extract [28] TiO2 25–87 (SEM) Spherical/anatase-rutile S. typhi, E. coli, and K. pneumoniae (broth micro dilution method)
Psidium guajava leaves extract [29] TiO(OH)2 32.58 (FESEM) Spherical shape and clusters/anatase-rutile S. aureus and E. coli (agar diffusion)
Vitex negundo Linn leaves extract [30] Ti{OCH(CH3)2}4 26–15 (TEM) Spherical and rod shaped/tetragonal phase anatase S. aureus and E. coli (agar diffusion)
Morinda citrifolia leaves extract [31] TiCl4 15–19 (SEM) Quasi-spherical shape/rutile S. aureus, B. subtilis, E. coli, P. aeruginosa, C. albicans, A. niger (agar diffusion)
Trigonella foenum-graecum leaf extract [21] TiOSO4 20–90 (HR-SEM) Spherical/anatase E. faecalis, S. aureus, S. faecalis, B. subtilis., Y. enterocolitica, P. vulgaris, E. coli, P. aeruginosa, K. pneumoniae, and C. albicans (agar diffusion)
Orange peel extract [32] TiCl4 20–50 (SEM) Irregular and angular structure with high porous net/anatase S. aureus, E. coli, and P. aeruginosa (agar diffusion)
Glycyrrhiza glabra root extracts [33] TiO2 60–140 (FESEM) Spherical shape/anatase S. aureus and K. pneumoniae (agar diffusion)

Table 1.

Synthesis of TiO2 NPs by using plant extracts.

Different factors need to be evaluated in this research field in order to obtain TiO2 NPs with better properties and to maintain their biocompatibility. It has been shown that nanoparticles obtained from green synthesis can have a better morphology and size translated into better antimicrobial activity. Mobeen and Sundaram have obtained TiO2 NPs from titanium tetrachloride precursor through a chemical and a green synthesis method. Sulfuric acid and ammonium hydroxide were used in the chemical-based method and, in the green synthesis, those chemical reagents were replaced by an orange peel extract [32]. The nanoparticles obtained by using the natural extract presented a well-defined and smaller crystalline nature (approx. 17.30 nm) compared to the nanoparticles synthesized through the chemical method (21.61 nm). Both methods resulted in anatase crystalline structures, and, when evaluating the antimicrobial activity, the more eco-friendly NPs revealed higher bactericidal activity against Gram-positive and Gram-negative bacteria compared to the chemically synthesized nanoparticles.

Bavanilatha et al. have also detailed TiO2 NPs green synthesis with Glycyrrhiza glabra root extract. Antibacterial activity against Staphylococcus aureus and Klebsiella pneumonia were investigated and in vivo toxicity tests using the zebrafish embryonic model (Danio rerio) were also carried out [33]. Results have demonstrated their biocompatibility because healthy embryos of adult fish to different variations of NP and no distinctive malformations were observed at every embryonic stage with respect to embryonic controls.

Subhapriya and Gomathipriya have biosynthesized TiO2 NPs by using a Trigonella foenum-graecum leaf extract, obtaining spherical NPs and their size varied between 20 and 90 nm, and their antimicrobial activity was evaluated through the standard method of disc diffusion [21]. The NPs showed significant antimicrobial activity against Yersinia enterocolitica (10.6 mm), Escherichia coli (10.8 mm), Staphylococcus aureus (11.2 mm), Enterococcus faecalis (11.4 mm), and Streptococcus faecalis (11.6 mm). Results confirmed developed TiO2 NPs as an effective antimicrobial drug that can lead to the progression of new antimicrobial drugs.

Spherical TiO2 NPs were synthesized from plants, in particular by applying a Morinda citrifolia leaf extract, and through advanced hydrothermal method [31]. Developed TiO2 NPs showed a size between 15 and 19 nm in an excellent quasispherical shape. In addition, their antimicrobial activity was tested against human pathogens, such as Staphylococcus aureus, Escherichia coli, Bacillus subtilis, Pseudomonas aeruginosa, Candida albicans, and Aspergillus niger. TiO2 NPs exhibited interesting antimicrobial activity, principally against Gram-positive bacteria.

In addition to plants, other organisms can produce inorganic compounds at an intra or extracellular level. The synthesis of TiO2 NPs through microorganisms, including bacteria, fungi, and yeasts, also meets the requirements and the exponentially growing technological demand toward eco-friendly strategies, by avoiding the use of toxic chemicals in the synthesis and protocols [34]. The metabolites generated by microorganism present bioreducing, capping, and stabilizing properties that improve the NPs synthesis performance. Jayaseelan et al. have stated glycyl-L-proline, one of the most abundant metabolite from Aeromonas hydrophilia bacteria, as the main compound that acted as a capping and stabilizing agent during TiO2 NPs green synthesis [35]. Moreover, the interest in fungi in green synthesis of metal oxide nanoparticles has increased over last years. Fungi enzymes and/or metabolites also present intrinsically the potential to obtain elemental or ionic state metals from their corresponding salts [34, 36]. Different works based on the green synthesis of TiO2 NPs from bacteria and fungus are presented in Table 2. Some of them have been synthesized with antimicrobial and antifungal purposes, and their target microorganisms are also declared.

Microorganism Titanium precursor Size (nm) Shape/crystal structure Target microorganisms (method)
Aeromonas hydrophilia [46] TiO(OH)2 28–54 (SEM) ~ 40.5 (XRD) Spherical/uneven S. aureus, S. pyogenes (agar diffusion)
Aspergillus flavus [34] TiO2 62–74 (TEM) Spherical/anatase and rutile E. coli, P. aeruginosa, K. pneumoniae, B. subtilis (agar diffusion and MIC)
Bacillus mycoides [37] Titanyl hydroxide 40–60 (TEM) Spherical/anatase E. coli (toxicity)
Bacillus subtilis [38] K2TiF6 11–32 (TEM) Spherical Aquatic biofilm
Fusarium oxysporum [36] K2TiF6 6–13 (TEM) Spherical/brookite —
Lactobacillus sp. [51] TiO(OH)2 ~ 24.6 (TEM) Spherical/anatase-rutile —
Planomicrobium sp. [39] TiO2 100–500 (SEM) Irregular/pure crystalline B. subtilis, K. planticola, Aspergillus niger (agar diffusion)
Propionibacterium jensenii [52] TiO(OH)2, 300°C 15–80 (FESEM) Spherical —
Saccharomyces cerevisiae [51] TiO(OH)2 ~ 12.6 (TEM) Spherical/anatase-rutile —

Table 2.

Examples of TiO2 NPs synthesis through microorganisms, both bacteria and fungus strains.

Two important factors that affect NPs synthesis are the type of microorganisms and their source. Some microorganisms widely used in the food industry are Lactobacillus, a bacterium used in dairy products and as a probiotic supplement, and Saccharomyces cerevisiae, a yeast commonly used in bakery. Jha et al. have investigated the effectiveness of both microorganisms to synthesize TiO2 NPs. A comparison between synthesis through Lactobacillus from yogurt and probiotic tablets resulted in different NP sizes: a particle size of 15–70 nm for yogurt, and 10–25 nm for tablets. This difference was due to the purity of the bacteria [40]. In general, TiO2 NP synthesis through microorganisms has not provided stable sizes, being not industrially scalable compared to the synthesis of nanoparticles from plants.

2.2 Antimicrobial activity of TiO2 NPs

Harmful bacteria, such as Staphylococcus aureus, Burkholderia cepacia, Pseudomonas aeruginosa, Clostridium difficile, Klebsiella pneumoniae, Escherichia coli, Acinetobacter baumannii, Mycobacterium tuberculosis, and Neisseria gonorrhoeae, are responsible for bacterial infections that can cause serious diseases in humans year after year [40]. The principal solution is the use of antibiotics, antimicrobial and antifungal agents. Nevertheless, in recent years there has been an increase in the resistance of several bacterial strains to these substances, and therefore there is currently a great interest in the search for new antimicrobial substances. The antimicrobial nanoparticles have been studied due to their high activity, specifically the metal oxide nanoparticles [41, 42, 43]. In this sense, titanium dioxide nanoparticles are one of the antimicrobial NPs whose study has gained interest during last years.

TiO2 is a thermally stable and biocompatible chemical compound with high photocatalytic activity and has presented good results against bacterial contamination [44]. Table 3 presents some research including the antimicrobial capacity of TiO2 NPs.

Microorganism NPs Results
Methicillin-resistant Staphylococcus aureus [45] Fe3O4-TiO2 core/shell magnetic NPs The survival ratio [%] of bacteria decreased from 82.40 to 7.13%.
Staphylococcus saprophyticus [45] Fe3O4-TiO2 core/shell magnetic NPs The survival ratio [%] of bacteria decreased from 79.15 to 0.51%.
Streptococcus pyogenes[57] Fe3O4-TiO2 core/shell magnetic NPs The survival ratio [%] of bacteria decreased from 82.87 to 4.45%.
Escherichia coli [46] TiO2 nanotubes
~ 20 nm		 97.53% of reduction
Staphylococcus aureus [46] TiO2 nanotubes
~ 20 nm		 99.94% of reduction
Bacillus subtilis [47] TiO2 NPs co-doped with silver (19–39 nm) 1% Ag-N-TiO2 had the highest antibacterial activity with antibacterial diameter reduction of 22.8 mm
Mycobacterium smegmatis [48] Cu-doped TiO2NPs
~20 nm		 The percentage of inhibition was around 47%
Pseudomonas aeruginosa [49] TiO2 NPs
10–25 nm		 Although it was not completely euthanized, their survival was significantly inhibited.
Shewanella oneidensis MR-1 [48] Cu-doped TiO2 NPs
~20 nm		 The percentage of inhibition was around 11%

Table 3.

TiO2 nanoparticles against different microorganisms and their antimicrobial activities.

The principal factors differentiating the antimicrobial activity between TiO2 NPs were their morphology, crystal nature, and size. According to López de Dicastillo et al. [11], hollow TiO2 nanotubes presented interesting antimicrobial reduction thanks to the enhancement of specific surface area. This fact can be explained by the nature of titanium dioxide, and one of the main mechanisms of its action is through the generation of reactive oxygen species (ROS) on its surface during the process of photocatalysis when it exposed to light at an appropriate wavelength. It is important to highlight that some research works have evidenced antimicrobial activity of TiO2 NPs increased when they were irradiated with UV-A light due to the photocatalytic nature of this oxide. The time of irradiation varied between 20 min [45] and 3 hours [50].

Advertisement

3. Understanding the antimicrobial mechanism of TiO2 NPs toward bacteria

Titanium dioxide nanoparticles (TiO2 NPs) are one of the most studied materials in the area of antimicrobial applications due to its particular abilities, such as bactericidal photocatalytic activity, safety, and self-cleaning properties. The mechanism referred to the antimicrobial action of TiO2 is commonly associated to reactive oxygen species (ROS) with high oxidative potentials produced under band-gap irradiation photo-induces charge in the presence of O2 [51]. ROS affect bacterial cells by different mechanisms leading to their death. Antimicrobial substances with broad spectrum activity against microorganisms (Gram-negative and Gram-positive bacteria and fungi) are of particular importance to overcome the MDR (multidrug resistance) generated by traditional antibiotic site-specific.

The main photocatalytic characteristic of TiO2 is a wide band gap of 3.2 eV, which can trigger the generation of high-energy electron–hole pair under UV-A light with wavelength of 385 nm or lower [52]. As mentioned above for bulk powder, TiO2 NPs have the same mechanism based on the ROS generation with the advantage of being at nanoscale. This nanoscale nature implies an important increase of surface area-to-volume ratio that provides maximum contact with environment water and oxygen [53] and a minimal size, which can easily penetrate the cell wall and cell membrane, enabling the increase of the intracellular oxidative damage.

Bacteria have enzymatic antioxidant defense systems like catalases and superoxide dismutase, in addition to natural antioxidants like ascorbic acid, carotene, and tocopherol, which inhibit lipid peroxidation or O-singlet and the effects of ROS radicals such as OH2˙− and OH˙. When those systems are exceeded, a set of redox reactions can lead to the death cell by the alteration of different essential structures (cell wall, cell membrane, DNA, etc.) and metabolism routes [54]. In the following sections, several ways that cellular structures were affected in the presence of TiO2 NPs will be described. In order to understand the genome responses of bacteria to TiO2-photocatalysis, some biological approaches related to expression of genes encoding to defense and repair mechanism of microorganism will explained below. Different mechanisms and processes of antimicrobial activity of TiO2 NPs are represented as a global scheme in Figure 1.

Figure 1.

Scheme of main antimicrobial activity-based processes.

3.1 Cell wall

ROS are responsible for the damage by oxidation of many organic structures of microorganisms. One of them is the cell wall, which is the first defense barrier against any injury from the environment, thus being the first affected by oxidative damage. Depending on the type of microorganism, the cell wall will have different composition; that is, in fungi and yeast, cell walls are mainly composed of chitin and polysaccharides [55], Gram-positive bacteria contain many layers of peptidoglycan and teichoic acid, and Gram-negative bacteria present a thin layer of peptidoglycan surrounded by a secondary lipid membrane reinforced with transmembrane lipopolysaccharides and lipoproteins [56]. Thus, the effect of TiO2 NPs will be slightly different depending type of microorganism.

It has been studied that the composition of the cell wall in Pichia pastoris (yeast) changed in the presence of TiO2, increasing the chitin content in response to the ROS effects [57]. The cell wall of Escherichia coli (Gram-negative) composed of lipo-polysaccharide, phosphatidyl-ethanolamine, and peptidoglycan has been reported to be sensitive to the peroxidation caused by TiO2 [58]. The damage can be quantified by assessing the production of malondialdehyde (MDA), which is a biomarker of lipid peroxidation, or through ATR-FTIR of the supernatant of cell culture, which evidenced the way that porins and proteins on the outer membrane were affected, probably as a result of greater exposure to the surface of TiO2 [59]. In fungi, the release of OH˙ captured hydrogen atoms from sugar subunits of polysaccharides, which composed the cell wall, leading to the cleavage of polysaccharide chain and the exposition of cell membrane [60].

In terms of genetic issues, there is evidence that the bacteria change the level expression of certain genes encoding for proteins involved in lipopolysaccharide and peptidoglycan metabolism, pilus biosynthesis, and protein insertion related to the cell wall which values were lower-expressed after exposition to TiO2 NPs [61].

3.2 Cell membrane

The second usual cellular target of most of antibiotics is the cell membrane mainly composed by phospholipids, which grant the cell a non-rigid cover, permeability, and protection. Most of the studies with TiO2 NPs have been focused to the loss of membrane integrity caused by oxidation of phospholipids due to ROS such hydroxyl radicals and hydrogen peroxide [62, 63], which led to an increase in the membrane fluidity, leakage of cellular content, and eventually cell lysis.

Gram-positive bacteria present only one membrane protected by many layers of peptidoglycan, whereas Gram-negative bacteria are composed by two membranes, inner and outer, and a thin layer of peptidoglycan between them. The outer membrane is exposed, thus, more liable to mechanical breakage due to the lack of peptidoglycan protective cover, like in Gram-positive bacteria [64]. Some studies have demonstrated a better antimicrobial performance of TiO2 NPs against Gram-positive bacteria [65] while others reported that Gram-negative bacteria were more resistant [66, 67]. It can be concluded that the bacterial inactivation effectiveness depends mainly on the resistant capacity of cell wall structures and the damage level of ROS generation [68].

In contrast with the lower expression of genes related to the cell wall seen before, the level expression of genes encoding for enzymes involved in metabolism of lipid essential for the cell membrane structure, are over-expressed [61]. It would be concluded that cells compensate the initial cell wall damage by reinforcing the second defense barrier, the cell membrane, in a way to provide support against the oxidation produced by ROS.

In fungi, the biocidal effect is not quite different. In the presence of TiO2 NPs and UV light, hydroxyl radicals, hydrogen peroxide, and superoxide anions initially promote oxidation of the membrane, leading to an unbalance in the cell permeability, even decomposition of cell walls [69]. This oxidation can inhibit cell respiration by affecting intracellular membranes in mitochondria. Studies have demonstrated biocidal effects on Penicillium expansum [70], but there is still research on other strains.

Beyond the relatively well-studied initial lipoperoxidation attack of TiO2 NPs on the outer/inner cell membrane of the microorganism, specific mechanisms are still aimed of being solved.

3.3 Inhibition of respiratory chain

As the oxidative damage generates lipoperoxidation of cell membranes due to their lipid nature, the respiratory chain, which takes place in the double-membrane mitochondria, is also affected. This organelle is a natural source of ROS in aerobic metabolism because superoxide anions are produced in the electron transfer respiratory chain process. Mitochondria can control this fact by converting them into H2O2 by superoxide dismutase (SOD), and finally into water by glutathione peroxidase and catalase [71]. The presence of TiO2 NPs increases the production of ROS at levels that this enzymatic defense mechanism cannot attenuate the damage, even a dysregulation in electron transfer through the mitochondrial respiratory chain implies an increase in ROS generation [72].

The genetic approaches have indicated that changes in level expression in genes related to the energy production in mitochondria prioritize the most efficient pathway to uptake oxygen, which is through ubiquinol coenzyme [61]. This coenzyme presented a higher capacity to exchange electrons, while the coenzyme-independent oxygen uptake pathways were expressed at lower level.

3.4 DNA

Damage at molecular level in DNA affects all regulatory microorganism metabolism, replication, transcription, and cell division. DNA is particularly sensitive to oxidative damage because oxygen radicals, specially OH˙ produced by Fenton reaction [73], may attack the sugar-phosphate or the nucleobases and cause saccharide fragmentation aimed to the strand break [74].

DNA strand modifications are more lethal than base modifications (punctual mutation). Mitochondrial DNA is more vulnerable to oxidative damage than nuclear DNA because it is closer to a major cellular ROS source [75].

Besides the enzymatic detoxification system (SOD, glutathione and catalase), DNA injuries are covered by a set of structures related to post-translational modification, protein turnover, chaperones (related to folding), DNA replication and repair, which are significantly over-expressed in the presence of TiO2 NPs [61].

3.5 Assimilation and transport of iron and inorganic phosphate (Pi)

Iron is an essential ion for cell growth and survival, but it can turn potentially toxic if some malfunction in homeostatic regulation occurs (i.e., Fenton reaction that produces ROS). Bacteria are able to regulate iron concentration in order to maintain it in a physiological range [76]. This regulation involves directly siderophores to active transport of iron in cell [77], whose coding genes related to siderophore synthesis and iron transport protein are significantly lower-expressed in the presence of TiO2 NPs, decreasing the ability to assimilate and transport it, leading to cell death [61]. The loss of homeostasis regulation was confirmed by ICP-MS analysis, which revealed that the presence of TiO2 NPs significantly reduced the cellular iron level in Pseudomonas brassicacearum, directly proportional to the cell viability [78].

Regarding the functions related to Pi group (PO4 3−) uptake, major differences were found in the expression of set of genes contained in Pho regulon, which were significantly lower when compared to the control [61]. The Pho regulon is a regulatory network in bacteria, yeast, plants, and animals, related to assimilation of inorganic phosphate, merely available in nature, and essential to nutritional cross-talk, secondary metabolite production, and pathogenesis [79].

This suggested that the microorganisms were highly deficient in phosphorus uptake and metabolism in the presence of TiO2 NPs. It should be also noted that the Pho regulon has been reported to regulate biofilm synthesis capacity and pathogenicity [80].

3.6 Cell-to-cell communication

TiO2 NPs can directly oxidize components of cell signaling pathways and even change the gene expression by interfering with transcription factors [81]. There is evidence to confirm the interference of TiO2 NPs in biosynthesis pathways of signaling molecules that bind lipopolysaccharide, stabilize and protect the cell wall against oxidative damage [82]. Moreover, a significant decrease in the synthesis of quorum-sensing signal molecule related to functions like pathogenesis and biofilm development was observed. This was corroborated through Scanning Electron Microscopy (SEM) images of bacteria (P. aeruginosa) growth in the presence of TiO2 NPs without UV irradiation. Cells appeared mainly non-aggregated and dispersed in the substratum, compared with controls without NPs where cells were mainly aggregated by lateral contact. This suggested that TiO2 NPs not only affected microorganisms by oxidative damage, but also bacteria aggregation and biofilm formation, which directly influenced in pathogenicity [83].

In plants and algae, ROS can act as signaling intermediates in the process of transcription factor controlling stress response by H2O2, which is activated by a GSH peroxidase, and not by peroxides directly. But there is still lack of research in this area [84].

Advertisement

4. Conclusions

The control of morphology and crystal structure of TiO2 NPs is the most important factor to enhance their antimicrobial activity. The appropriate design based on desirable surface properties given by shaped nanoparticles can improve effectiveness that is also dependent on the type of bacteria. The route of synthesis of TiO2 NPs is also a key factor. Recent works have revealed more eco-friendly synthesis methods, principally based on plant-based compounds and microorganisms, such as bacteria and fungus. Antimicrobial activity of different TiO2 NPs against Gram-positive and Gram-negative bacteria including antibiotic-resistant strains has been confirmed in different works.

Specific studies on antimicrobial mechanisms have evidenced that microorganism exposed to photocatalytic TiO2 NPs exhibited cell inactivation at regulatory network and signaling levels, an important decrease in the activity of respiratory chain, and inhibition in the ability to assimilate and transport iron and phosphorous. These processes with the extensive cell wall and membrane alterations were the main factors that explain the biocidal activity of TiO2 NPs.

Advertisement

Acknowledgments

The authors acknowledge the financial support of CONICYT through the Project Fondecyt Regular 1170624 and “Programa de Financiamiento Basal para Centros Científicos y Tecnológicos de Excelencia” Project FB0807, and CORFO Project 17CONTEC-8367.

Advertisement

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1. Hajipour MJ, Fromm KM, Akbar Ashkarran A, Jimenez de Aberasturi D, de Larramendi IR, Rojo T, et al. Antibacterial properties of nanoparticles. Trends in Biotechnology. 2012;30:499-511. DOI: 10.1016/j.tibtech.2012.06.004
  2. 2. Whitesides G. Nanoscience, nanotechnology, and chemistry. Small. 2005;1:172-179. DOI: 10.1002/smll.200400130
  3. 3. Khan SUM, Al-Shahry M, Ingler WB. Efficient photochemical water splitting by a chemically modified n-TiO2. Science. 2002;297:2243-2245. DOI: 10.1126/science.1075035.
  4. 4. Chung IM, Park I, Seung-Hyun K, Thiruvengadam M, Rajakumar G. Plant-mediated synthesis of silver nanoparticles: Their characteristic properties and therapeutic applications. Nanoscale Research Letters. 2016;11:1-14. DOI: 10.1186/s11671-016-1257-4
  5. 5. Bui AKT, Bacic A, Pettolino F. Polysaccharide composition of the fruit juice of Morinda citrifolia (noni). Phytochemistry. 2006;67:1271-1275. DOI: 10.1016/j.phytochem.2006.04.023
  6. 6. Ravikumar P, Kumar SS. Antifungal activity of extracellularly synthesized silver nanoparticles from Morinda citrifolia L. International Journal of Technical Research and Applications. 2014;2:108-111
  7. 7. Inbathamizh L, Ponnu TM, Mary EJ. In vitro evaluation of antioxidant and anticancer potential of Morinda pubescens synthesized silver nanoparticles. Journal of Pharmacy Research. 2013;6:32-38. DOI: 10.1016/j.jopr.2012.11.010
  8. 8. De Oliveira RC, de Foggi CC, Teixeira MM, Da Silva MDP, Assis M, Francisco EM, et al. Mechanism of antibacterial activity via morphology change of α-AgVO3: Theoretical and experimental insights. ACS Applied Materials & Interfaces. 2017;9:11472-11481. DOI: 10.1021/acsami.7b00920
  9. 9. Pal S, Tak YK, Song JM. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Applied and Environmental Microbiology. 2007;73:1712-1720. DOI: 10.1128/AEM.02218-06
  10. 10. Gilbertson LM, Albalghiti EM, Fishman ZS, Perreault F, Corredor C, Posner JD, et al. Shape-dependent surface reactivity and antimicrobial activity of nano-cupric oxide. Environmental Science & Technology. 2016;50:3975-3984. DOI: 10.1021/acs.est.5b05734
  11. 11. López de Dicastillo C, Patiño C, Galotto MJ, Palma JL, Alburquenque D, Escrig J. Novel antimicrobial titanium dioxide nanotubes obtained through a combination of atomic layer deposition and electrospinning technologies. Nanomaterials. 2018;8:128. DOI: 10.3390/nano8020128
  12. 12. He Z, Cai Q , Fang H, Situ G, Qiu J, Song S, et al. Photocatalytic activity of TiO2 containing anatase nanoparticles and rutile nanoflower structure consisting of nanorods. Journal of Environmental Sciences. 2013;25:2460-2468. DOI: 10.1016/S1001-0742(12)60318-0
  13. 13. Sarkar D, Ghosh CK, Chattopadhyay KK. Morphology control of rutile TiO2 hierarchical architectures and their excellent field emission properties. CrystEngComm. 2012;14:2683-2690. DOI: 10.1039/c2ce06392a
  14. 14. Burda C, Chen X, Narayanan R, El-Sayed MA. Chemistry and properties of nanocrystals of different shapes. Chemical Reviews. 2005;105:1025-1102. DOI: 10.1021/cr030063a
  15. 15. Zhang Q , Yan X, Shao R, Dai H, Li S. Preparation of nano-TiO2 by liquid hydrolysis and characterization of its antibacterial activity. Journal Wuhan University of Technology, Materials Science Edition. 2014;29:407-409. DOI: 10.1007/s11595-014-0930-7
  16. 16. Vimbela GV, Ngo SM, Fraze C, Yang L, Stout DA. Antibacterial properties and toxicity from metallic nanomaterials. International Journal of Nanomedicine. 2017;12:3941-3965. DOI: 10.2147/IJN.S134526
  17. 17. Puzyn T, Rasulev B, Gajewicz A, Hu X, Dasari TP, Michalkova A, et al. Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles. Nature Nanotechnology. 2011;6:175-178. DOI: 10.1038/nnano.2011.10
  18. 18. He X, Fu P, Aker WG, Hwang HM. Toxicity of engineered nanomaterials mediated by nano–bio–eco interactions. Journal of Environmental Science and Health - Part C Environmental Carcinogenesis and Ecotoxicology Reviews. 2018;36:21-42. DOI: 10.1080/10590501.2017.1418793
  19. 19. Hwang HM, Ray PC, Yu H, He X. Toxicology of designer/engineered metallic nanoparticles. In book: Sustainable preparation of metal nanoparticles. 2012:190-212. Chapter 8. DOI: 10.1039/9781849735469-00190
  20. 20. Shah M, Fawcett D, Sharma S, Tripathy SK, Poinern GEJ. Green synthesis of metallic nanoparticles via biological entities. Materials. 2015;8:7278-7308. DOI: 10.3390/ma8115377
  21. 21. Subhapriya S, Gomathipriya P. Green synthesis of titanium dioxide (TiO2) nanoparticles by Trigonella foenum-graecum extract and its antimicrobial properties. Microbial Pathogenesis. 2018;116:215-220. DOI: 10.1016/j.micpath.2018.01.027
  22. 22. Bali R, Razak N, Lumb A, Harris AT. The synthesis of metallic nanoparticles inside live plants. In: Proc. 2006 Int. Conf. Nanosci. Nanotechnology, ICONN. 2006. pp. 224-227. DOI: 10.1109/ICONN.2006.340592
  23. 23. Moghaddam AB, Moniri M, Azizi S, Rahim RA, Bin AA, Saad WZ, et al. Biosynthesis of ZnO nanoparticles by a new Pichia kudriavzevii yeast strain and evaluation of their antimicrobial and antioxidant activities. Molecules. 2017;22(6):872. DOI: 10.3390/molecules22060872
  24. 24. Jha Z, Behar N, Narayan Sharma S, Chandel G, Sharma D, Pandey MP, et al. Nanotechnology: Prospects of agricultural advancement. Nano Vision. 2011;1:88-100
  25. 25. Jose Varghese R, Zikalala N, Sakho EHM, Oluwafemi OS. Green synthesis protocol on metal oxide nanoparticles using plant extracts. Colloidal Metal Oxide Nanoparticles. 2020:67-82. Chapter 5. DOI: 10.1016/B978-0-12-813357-6.00006-1
  26. 26. Nasrollahzadeh M, Maham M, Mohammad Sajadi S. Green synthesis of CuO nanoparticles by aqueous extract of Gundelia tournefortii and evaluation of their catalytic activity for the synthesis of N-monosubstituted ureas and reduction of 4-nitrophenol. Journal of Colloid and Interface Science. 2015;455:245-253. DOI: 10.1016/j.jcis.2015.05.045
  27. 27. Nadeem M, Tungmunnithum D, Hano C, Abbasi BH, Hashmi SS, Ahmad W, et al. The current trends in the green syntheses of titanium oxide nanoparticles and their applications. Green Chemistry Letters and Reviews. 2018;11:492-502. DOI: 10.1080/17518253.2018.1538430
  28. 28. Thakur BK, Kumar A, Kumar D. Green synthesis of titanium dioxide nanoparticles using Azadirachta indica leaf extract and evaluation of their antibacterial activity. South African Journal of Botany. 2019;124:223-227. DOI: 10.1016/j.sajb.2019.05.024
  29. 29. Santhoshkumar T, Rahuman AA, Jayaseelan C, Rajakumar G, Marimuthu S, Kirthi AV, et al. Green synthesis of titanium dioxide nanoparticles using Psidium guajava extract and its antibacterial and antioxidant properties. Asian Pacific Journal of Tropical Medicine. 2014;7:968-976. DOI: 10.1016/S1995-7645(14)60171-1
  30. 30. Ambika S, Sundrarajan M. [EMIM] BF 4 ionic liquid-mediated synthesis of TiO2 nanoparticles using Vitex negundo Linn extract and its antibacterial activity. Journal of Molecular Liquids. 2016;221:986-992. DOI: 10.1016/j.molliq.2016.06.079
  31. 31. Sundrarajan M, Bama K, Bhavani M, Jegatheeswaran S, Ambika S, Sangili A, et al. Obtaining titanium dioxide nanoparticles with spherical shape and antimicrobial properties using M. citrifolia leaves extract by hydrothermal method. Journal of Photochemistry and Photobiology B: Biology. 2017;171:117-124. DOI: 10.1016/j.jphotobiol.2017.05.003
  32. 32. Mobeen Amanulla A, Sundaram R. Green synthesis of TiO2 nanoparticles using orange peel extract for antibacterial, cytotoxicity and humidity sensor applications. Materials Today Proceedings. 2019;8:323-331. DOI: 10.1016/j.matpr.2019.02.118
  33. 33. Bavanilatha M, Yoshitha L, Nivedhitha S, Sahithya S. Bioactive studies of TiO2 nanoparticles synthesized using Glycyrrhiza glabra. Biocatalysis and Agricultural Biotechnology. 2019;19:101131. DOI: 10.1016/j.bcab.2019.101131
  34. 34. Rajakumar G, Rahuman AA, Roopan SM, Khanna VG, Elango G, Kamaraj C, et al. Fungus-mediated biosynthesis and characterization of TiO2 nanoparticles and their activity against pathogenic bacteria. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy. 2012;91:23-29. DOI: 10.1016/J.SAA.2012.01.011
  35. 35. Jayaseelan C, Rahuman AA, Roopan SM, Kirthi AV, Venkatesan J, Kim SK, et al. Biological approach to synthesize TiO2 nanoparticles using Aeromonas hydrophila and its antibacterial activity. Spectrochimica Acta - Part A: Molecular and Biomolecular Spectroscopy. 2013;107:82-89. DOI: 10.1016/j.saa.2012.12.083
  36. 36. Bansal V, Rautaray D, Bharde A, Ahire K, Sanyal A, Ahmad A, et al. Fungus-mediated biosynthesis of silica and titania particles. Journal of Materials Chemistry. 2005;15:2583. DOI: 10.1039/b503008k
  37. 37. Órdenes-Aenishanslins NA, Saona LA, Durán-Toro VM, Monrás JP, Bravo DM, Pérez-Donoso JM. Use of titanium dioxide nanoparticles biosynthesized by Bacillus mycoides in quantum dot sensitized solar cells. Microbial Cell Factories. 2014;13:90. DOI: 10.1186/s12934-014-0090-7
  38. 38. Dhandapani P, Maruthamuthu S, Rajagopal G. Bio-mediated synthesis of TiO2 nanoparticles and its photocatalytic effect on aquatic biofilm. Journal of Photochemistry and Photobiology B: Biology. 2012;110:43-49. DOI: 10.1016/j.jphotobiol.2012.03.003
  39. 39. Sinica DP, Annadurai G. Pelagia research library novel eco-friendly synthesis of titanium oxide nanoparticles by using Planomicrobium sp. and its antimicrobial evaluation. Der Pharmacia. 2013;4:59-66
  40. 40. Jha AK, Prasad K. Biosynthesis of metal and oxide nanoparticles using lactobacilli from yoghurt and probiotic spore tablets. Biotechnology Journal. 2010;5:285-291. DOI: 10.1002/biot.200900221
  41. 41. Raja S, Ramesh V, Thivaharan V. Green biosynthesis of silver nanoparticles using Calliandra haematocephala leaf extract, their antibacterial activity and hydrogen peroxide sensing capability. Arabian Journal of Chemistry. 2017;10:253-261. DOI: 10.1016/j.arabjc.2015.06.023
  42. 42. Müller JC, Botelho GGK, Bufalo AC, Boareto AC, Rattmann YD, Martins ES, et al. Morinda citrifolia Linn (noni): In vivo and in vitro reproductive toxicology. Journal of Ethnopharmacology. 2009;121:229-233. DOI: 10.1016/j.jep.2008.10.019
  43. 43. Pai AR, Kavitha S, Shweta Raj S, Priyanka P, Vrinda A, Vivin TS, et al. Green synthesis and characterizations of silver nanoparticles using fresh leaf extract of Morinda citrifolia and its anti-microbial activity studies. International Journal of Pharmacy and Pharmaceutical Sciences. 2015;7:459-461
  44. 44. Ma W, Li J, Liu Y, Ren X, Gu ZG, Xie Z, et al. Preparation and characterization of excellent antibacterial TiO2/N-halamines nanoparticles. Colloids and Surfaces A: Physicochemical and Engineering Aspects. 2016;506:284-290. DOI: 10.1016/j.colsurfa.2016.06.055
  45. 45. Chen W-J, Tsai P-J, Chen Y-C. Functional Fe3O4/TiO2 core/shell magnetic nanoparticles as photokilling agents for pathogenic bacteria. Small. 2008;4:485-491. DOI: 10.1002/smll.200701164
  46. 46. Podporska-Carroll J, Panaitescu E, Quilty B, Wang L, Menon L, Pillai SC. Antimicrobial properties of highly efficient photocatalytic TiO2 nanotubes. Applied Catalysis B: Environmental. 2015;176-177:70-75. DOI: 10.1016/j.apcatb.2015.03.029
  47. 47. Yuan Y, Ding J, Xu J, Deng J, Guo J. TiO2 nanoparticles co-doped with silver and nitrogen for antibacterial application. Journal of Nanoscience and Nanotechnology. 2010;10:4868-4874. DOI: 10.1166/jnn.2010.2225
  48. 48. Wu B, Huang R, Sahu M, Feng X, Biswas P, Tang YJ. Bacterial responses to Cu-doped TiO2 nanoparticles. Science of the Total Environment. 2010;408:1755-1758. DOI: 10.1016/j.scitotenv.2009.11.004
  49. 49. Tsuang Y-H, Sun J-S, Huang Y-C, Lu C-H, Chang WH-S, Wang C-C. Studies of photokilling of bacteria using titanium dioxide nanoparticles. Artificial Organs. 2008;32:167-174. DOI: 10.1111/j.1525-1594.2007.00530.x
  50. 50. López de Dicastillo C, Patiño C, Galotto MJ, Vásquez-Martínez Y, Torrent C, Alburquenque D, et al. Novel hollow titanium dioxide nanospheres with antimicrobial activity against resistant bacteria. Beilstein Journal of Nanotechnology. 2019;10:1716-1725. DOI: 10.3762/bjnano.10.167
  51. 51. Verdier T, Coutand M, Bertron A, Roques C. Antibacterial activity of TiO2 photocatalyst alone or in coatings on E. coli: The influence of methodological aspects. Coatings. 2014;4:670-686. DOI: 10.3390/coatings4030670
  52. 52. Xie J, Hung YC. Methodology to evaluate the antimicrobial effectiveness of UV-activated TiO2 nanoparticle-embedded cellulose acetate film. Food Control. 2019;106:106690. DOI: 10.1016/j.foodcont.2019.06.016
  53. 53. Kaladhar Reddy A, Kambalyal PB, Shanmugasundaram K, Rajesh V, Donthula S, Patil SR. Comparative evaluation of antimicrobial efficacy of silver, titanium dioxide and zinc oxide nanoparticles against streptococcus mutans. Pesquisa Brasileira Em Odontopediatria e Clinica Integrada. 2018;18:1-8. DOI: 10.4034/PBOCI.2018.181.88
  54. 54. Kiwi J, Rtimi S. Mechanisms of the antibacterial effects of TiO 2 -FeO x under solar or visible light: Schottky barriers versus surface plasmon resonance. Coatings. 2018;8:391. DOI: 10.3390/coatings8110391
  55. 55. Gow NAR, Latge J-P, Munro CA. The fungal Cell Wall: Structure, biosynthesis, and function. Microbiology Spectrum. 2017;5(3):1-25. DOI: 10.1128/microbiolspec.FUNK-0035-2016
  56. 56. Salton MRJ, Kim K-S. Structure. Galveston: University of Texas Medical Branch; 1996
  57. 57. Liu Z, Zhang M, Han X, Xu H, Zhang B, Yu Q , et al. TiO2 nanoparticles cause cell damage independent of apoptosis and autophagy by impairing the ROS-scavenging system in Pichia pastoris. Chemico-Biological Interactions. 2016;252:9-18. DOI: 10.1016/j.cbi.2016.03.029
  58. 58. Pulgarin C, Kiwi J, Nadtochenko V. Mechanism of photocatalytic bacterial inactivation on TiO2 films involving cell-wall damage and lysis. Applied Catalysis B: Environmental. 2012;128:179-183. DOI: 10.1016/j.apcatb.2012.01.036
  59. 59. Carré G, Hamon E, Ennahar S, Estner M, Lett MC, Horvatovich P, et al. TiO2 photocatalysis damages lipids and proteins in Escherichia coli. Applied and Environmental Microbiology. 2014;80:2573-2581. DOI: 10.1128/AEM.03995-13
  60. 60. Hammel KE, Kapich AN, Jensen KA, Ryan ZC. Reactive oxygen species as agents of wood decay by fungi. Enzyme and Microbial Technology. 2002;30:445-453. DOI: 10.1016/S0141-0229(02)00011-X
  61. 61. Kubacka A, Diez MS, Rojo D, Bargiela R, Ciordia S, Zapico I, et al. Understanding the antimicrobial mechanism of TiO 2 -based nanocomposite films in a pathogenic bacterium. Scientific Reports. 2014;4:1-9. DOI: 10.1038/srep04134
  62. 62. Pavlović VP, Vujančević JD, Mašković P, Ćirković J, Papan JM, Kosanović D, et al. Structure and enhanced antimicrobial activity of mechanically activated nano TiO2. Journal of the American Ceramic Society. 2019;102:7735-7745. DOI: 10.1111/jace.16668
  63. 63. Khezerlou A, Alizadeh-Sani M, Azizi-Lalabadi M, Ehsani A. Nanoparticles and their antimicrobial properties against pathogens including bacteria, fungi, parasites and viruses. Microbial Pathogenesis. 2018;123:505-526. DOI: 10.1016/j.micpath.2018.08.008
  64. 64. Jameel ZN, Mahmood OA, Ahmed FL. Studying the effect of synthesized nano-titanium dioxide via two phases on the Pseudomonas aeruginosa and portus bacteria as antimicrobial agents. International Journal of Nanoelectronics and Materials. 2019;12:329-338
  65. 65. Cheigh C-I, Park M-H, Chung M-S, Shin J-K, Park Y-S. Comparison of intense pulsed light- and ultraviolet (UVC)-induced cell damage in Listeria monocytogenes and Escherichia coli O157:H7. Food Control. 2012;25:654-659. DOI: 10.1016/J.FOODCONT.2011.11.032
  66. 66. Dunlop PSM, Sheeran CP, Byrne JA, McMahon MAS, Boyle MA, McGuigan KG. Inactivation of clinically relevant pathogens by photocatalytic coatings. Journal of Photochemistry and Photobiology A: Chemistry. 2010;216:303-310. DOI: 10.1016/J.JPHOTOCHEM.2010.07.004
  67. 67. van Grieken R, Marugán J, Pablos C, Furones L, López A. Comparison between the photocatalytic inactivation of Gram-positive E. faecalis and Gram-negative E. coli faecal contamination indicator microorganisms. Applied Catalysis B: Environmental. 2010;100:212-220. DOI: 10.1016/J.APCATB.2010.07.034
  68. 68. Zhu Z, Cai H, Sun DW. Titanium dioxide (TiO2) photocatalysis technology for nonthermal inactivation of microorganisms in foods. Trends in Food Science and Technology. 2018;75:23-35. DOI: 10.1016/j.tifs.2018.02.018
  69. 69. Li J, Yu H, Wu Z, Wang J, He S, Ji J, et al. Room temperature synthesis of crystalline anatase TiO2 on bamboo timber surface and their short-term antifungal capability under natural weather conditions. Colloids and Surfaces A: Physicochemical and Engineering Aspects. 2016;508:117-123. DOI: 10.1016/j.colsurfa.2016.08.045
  70. 70. Maneerat C, Hayata Y. Antifungal activity of TiO2 photocatalysis against Penicillium expansum in vitro and in fruit tests. International Journal of Food Microbiology. 2006;107:99-103. DOI: 10.1016/j.ijfoodmicro.2005.08.018
  71. 71. Staerck C, Gastebois A, Vandeputte P, Calenda A, Larcher G, Gillmann L, et al. Microbial antioxidant defense enzymes. Microbial Pathogenesis. 2017;110:56-65. DOI: 10.1016/J.MICPATH.2017.06.015
  72. 72. Xue C, Li X, Liu G, Liu W. Evaluation of mitochondrial respiratory chain on the generation of reactive oxygen species and cytotoxicity in HaCaT cells induced by Nanosized titanium dioxide under UVA irradiation. International Journal of Toxicology. 2016;35:644-653. DOI: 10.1177/1091581816661853
  73. 73. Gogniat G, Dukan S. TiO2 photocatalysis causes DNA damage via Fenton reaction-generated hydroxyl radicals during the recovery period. Applied and Environmental Microbiology. 2007;73:7740-7743. DOI: 10.1128/AEM.01079-07
  74. 74. Imlay J, Linn S. Damage and oxygen radical. Science. 1988;240:1302-1309
  75. 75. Ševců A, El-Temsah YS, Joner EJ, Černík M. Oxidative stress induced in microorganisms by zero-valent iron nanoparticles. Microbes and Environments. 2011;26:271-281. DOI: 10.1264/jsme2.me11126
  76. 76. Andrews SC, Robinson AK, Rodríguez-Quiñones F. Bacterial iron homeostasis. FEMS Microbiology Reviews. 2003;27:215-237. DOI: 10.1016/S0168-6445(03)00055-X
  77. 77. Neilands JB. Siderophores of bacteria and fungi. Microbiological Sciences. 1984;1:9-14
  78. 78. Liu W, Bertrand M, Chaneac C, Achouak W. TiO2 nanoparticles alter iron homeostasis in: Pseudomonas brassicacearum as revealed by PrrF sRNA modulation. Environmental Science: Nano. 2016;3:1473-1482. DOI: 10.1039/c6en00316h
  79. 79. Santos-Beneit F. The pho regulon: A huge regulatory network in bacteria. Frontiers in Microbiology. 2015;6:402. DOI: 10.3389/fmicb.2015.00402
  80. 80. Haddad A, Jensen V, Becker T, Hãussler S. The pho regulon influences biofilm formation and type three secretion in Pseudomonas aeruginosa. Environmental Microbiology Reports. 2009;1:488-494. DOI: 10.1111/j.1758-2229.2009.00049.x
  81. 81. Apel K, Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology. 2004;55:373-399. DOI: 10.1146/annurev.arplant.55.031903.141701
  82. 82. Johnson L, Mulcahy H, Kanevets U, Shi Y, Lewenza S. Surface-localized Spermidine protects the Pseudomonas aeruginosa outer membrane from antibiotic treatment and oxidative stress. Journal of Bacteriology. 2012;194:813-826. DOI: 10.1128/JB.05230-11
  83. 83. Kubacka A, Serrano C, Ferrer M, Lunsdorf H, Bielecki P, Cerrada ML, et al. High-performance dual-action polymer-TiO2 nanocomposite films via melting processing. Nano Letters. 2007;7:2529-2534. DOI: 10.1021/nl0709569
  84. 84. Ledford HK, Niyogi KK. Singlet oxygen and photo-oxidative stress management in plants and algae. Plant, Cell and Environment. 2005;28:1037-1045. DOI: 10.1111/j.1365-3040.2005.01374.x

Written By

Carol López de Dicastillo, Matias Guerrero Correa, Fernanda B. Martínez, Camilo Streitt and Maria José Galotto

Submitted: 31 August 2019 Reviewed: 18 December 2019 Published: 27 January 2020

© 2020 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Continue reading from the same book

View All
Chapter 6 Dairy Farms Biosecurity to Protect against Infecti...

By Stelian Baraitareanu and Livia Vidu

1300 downloads

Chapter 7 Antimicrobial Resistance with Special Emphasis on ...

By Nitya Meenakshi Raman, Murugesh Easwaran, Rashmi K...

992 downloads

Chapter 8 Of Animal and Men: The Importance of Animal Enviro...

By Miliane Moreira Soares de Souza, Cláudio Marcos Ro...

913 downloads