Reduction potential standard for different chemical species [36–38].
Actinobacteria, such as Mycobacterium, that constitute one of the main phyla within the bacteria and some genus of this phylum are reported to be a pathogen of or associated with nosocomial infections and pseudoinfections promoting health risks for immunocompromised people, particularly AIDS patients. They are also related to lower quality of surface water due to their odor production (Actinomycineae and Streptomycetaceae). These bacteria have been isolated from hospital water distribution systems, municipal drinking water, freshwater, and among other environmental samples. Their biofilm formation, amoeba-associated lifestyle, and resistance to chlorine/ozone have been recognized as important factors that contribute to persistence of these bacteria in water distribution systems. Research for new disinfection methods that are able to promote complete inactivation of these bacteria has currently increased. Among them is the use of advanced oxidation process that has demonstrated promising results; the production of ⋅OH radicals with high oxidizing power are capable to kill bacteria and can also destroy the products generated from lyse cell. The goal of the present work is to review the main processes based on advanced oxidation process that are able to promote actinobacterium disinfection. The fundaments of this process are also reviewed. Special emphasis was done for the photocatalysis and photoelectrocatalysis methods and the phenomena occurring at the electrode/electrolyte interface.
Actninobacteria or actinomycetes constitute a vast phylum within the domain Bacteria and is formed by bacteria with high content of guanine and cytosine in the DNA [1–3]. Actinobacteria have some similarities with the microorganisms of the domain Fungi, such as the formation of hyphal and spore dissemination. However, the absence of nuclear membrane, the presence of the typical bacterial flagellum, and sensitivity to antibiotics provided the migration of actinobacteria to the domain Bacteria .
There are various different lifestyles among
They are widely distributed in terrestrial  and freshwater environmentals . The initial hierarchical classification system of
Mycobacteria are a genus belonging to the class of Actinomycetes and are among the most important microorganism pathogens, causing diseases such as leprosy and tuberculosis. Although it has been more than 100 years since the discovery of its etiological agents, these diseases are still associated with high levels of morbidity and mortality, respectively [7, 8]. These bacteria usually occur as straight or slightly curved rods, although they may also appear in the form of hyphae that are fragmented in coccoid elements or rods. Although considered as Gram-positive bacteria, studies confirm the presence of an external membrane in the mycobacterial envelope, resembling in this respect a Gram-negative bacteria . Another outstanding feature for mycobacteria is the significant presence of mycolic acids in the cell wall, forming a waxy, water resistant layer, making for a great resistance to adverse conditions such as dryness. In addition, mycolic acids are also responsible for alcohol- and acid-resistance, another outstanding feature of this genus .
The two major human mycobacteriosis are leprosy and tuberculosis, caused by
It is important to note that not all actinobacteria are pathogenic. It is highlighted that the genus
The presence of
2. Occurrence of actinobacterium in water samples
The nature of the microbiology of tap water delivered to consumers via public drinking water distribution systems has been studied by Holinger et al. . The authors studied tap water from 17 different cities between the headwaters of the Arkansas River and the mouth of the Mississippi River. The occurrence of Actinobacteria was detected in 24% of the samples, of which 85% were
The presence of mycobacteria has also been reported in municipal drinking water distribution systems, hospital water systems, and in ice machines, swimming pools, and whirlpools [17–21].
Klanicova et al.  have analyzed 124 samples of four drinking water supply systems in the Czech Republic, 52 dam sediments, 34 water treatment plant sludge samples, and 38 tap water household sediments. Actinobacteria of 11 different species were isolated by culture from 42 (33.9%) samples; the most prevalent were
The analysis of freshwater lakes in China showed the bacterial diversity and were identified as Proteobacteria (40.9%), followed by Actinobacteria (15.9%), Cyanobacteria (11.4%), Verrucomicrobia (11.4%), Plantomycetes (6.8%), Bacteroidetes (4.5%), and Chloroflexi (4.5%) . The investigation of the composition and diversity of biofilm bacterial community present in real drinking water distribution systems (DWDSs) with different purification strategies (conventional treatment and integrated treatment) show that actinobacteria is the major component of the biofilm bacterial community . The abundance, identity, and activity of uncultured actinobacterium present in a drinking water reservoir (North Pine Dam, Brisbane, Australia) has also been shown . The structures and dynamics of bacterial communities from raw source water, groundwater, and drinking water before and after filtration were studied in four seasons of a year. The bacterial communities of different seasons from the four sampling sites were clustered into two major groups: water before and after filtration and source water and groundwater; representatives of the phyla Actinobacteria were found at all four sampling sites .
Analysis of bacterial communities associated with different drinking water treatment processes (e.g., coagulation, sedimentation, sand filtration, and chloramine disinfection) and from distantly piped water showed a large proportion of the phyla Actinobacteria and Bacteroidetes. The piped water exhibited increasing taxonomic diversity, including human pathogens such as the
The presence of NTM was also reported in waters of a hemodialysis center . Analysis of 210 samples of water from the hydric system of the unit (post-osmosis system, hemodialysis rooms, reuse system, and hemodialysis equipment) and from the municipal supply network was studied. The results showed that 24.3% of the collected samples tested positive for NTM; both the municipal supply network (2 samples, 3.2%) and the hydric system of the hemodialysis center (49 samples, 96.1%) contained NTM. Among the mycobacteria isolated, the authors highlight the presence of
The incidence of NTM was also obtained in hot water systems of hospital settings with disinfection using hydrogen peroxide and silver; thermal disinfection or chlorine dioxide showed the persistence of NTM in 47% of the samples, equivalent to the remaining concentration between 10–1625 CFU L-1. Among the NTM species that were isolated are
It was confirmed that drinking water supply systems (watershed–reservoir–drinking water treatment plant–household) might be a potential transmission route for actinobacteria, where mycobacteria are most reported. Some of these mycobacteria can cause various disseminated infections, tuberculosis-like illnesses, lymphadenitis, osteomyelitis in animals and in immunocompromised humans, paratuberculosis (Johne’s disease), and chronic enteritis in ruminants .
The abundance of the above-mentioned microorganisms in water could stem from their biofilm formation, amoeba-associated lifestyle, and resistance to chlorine, which have been recognized as important factors that contribute to the survival, colonization, and persistence of actinobacteria in water distribution systems. The presence of actinobacterium in tap water, mainly mycobacteria, has been linked to nosocomial infections and pseudoinfections and provides a health risk for immunocompromised people, particularly AIDS patients. The research for new disinfection methods has been increasing and among them, the use of advanced oxidation process has been give promising results.
3. Advanced Oxidation Processes (AOPs): Basic concepts
Chemical oxidation may be defined as a reaction in which electrons are removed from a substance, increasing their oxidation state . The reactions involving oxidizing agents, such as H2O2 and O3, are thermodynamically favored. However, they can be kinetically slow. In the presence of highly-oxidizing free radicals, such as hydroxyl radicals (⋅OH), could be found reaction rates of a million to a billion times faster compared with the oxidizing agents mentioned above . Thus, the generation of hydroxyl radicals (⋅OH) is an essential step in the efficiency of advanced oxidation processes . They are formed via the oxidation of water on the anode surface, as shown in Equation 1.
These chemical species are effective in destroying organic chemicals because they are reactive electrophiles (electron preferring), which react rapidly and are non-selective in relation to all electron-rich organic compounds [33, 34]. Furthermore, these react unselectively with a wide range of recalcitrant organics, often at diffusion-limited rates [35–38].
Table 1 lists the standard reduction potential of some oxidants. It is observed that the radical ⋅OH is a strong oxidant, only lower than fluoride, surpassing O3 and H2O2.
For the generation of hydroxyl radicals in a reaction medium, there are different methods to classify them as homogenous and heterogeneous, and they may occur with or without light irradiation. Homogeneous systems are characterized by the absence of a solid catalyst utilized to initiate the reaction. In contrast, heterogeneous processes make use of solid catalysts to contribute to the formation of hydroxyl radicals . Figure 1 summarizes the most common of AOPs systems.
Among the different AOPs systems, heterogeneous catalysis has received prominence over the years. Photocatalytic oxidation can be a good option for water disinfection, its performance is greatly restricted by fast electron-hole (e/h+) recombination. The strategy to increase photocatalytic efficiency is photoelectrocatalysis (PEC), which consists of introducing a reverse bias potential to the anode coated with the photocatalyst [40–42]. The PEC process minimizes recombination, this process exists under bias potential, creating the potential gradient on the anode that is enough to remove the electrons from the conduction band to an external counter electrode. This increases the availability of ⋅OH radicals and other reactive oxygen species (ROS), which can attack the bacterium cell wall and organics compounds when the bacteria gets in contact with the catalyst .
The principle of photocatalysis is based on the activation of a semiconductor (commonly titanium dioxide (TiO2)) by light irradiation. In order for the semiconductor to become a conductive material, charge carriers need to be created, usually by photoexcitation. The principle of the process is the generation of a pair of electron/hole (e-/h+) by promotion of an electron from the valence band (VB) to the conduction band (CB) (Equation 2). A semiconductor material is characterized by the presence of a VB and a CB separated by a band gap energy (Eg) . Figure 2 shows a schematic representation of a photoexcited semiconductor.
In a semicondutor, the Fermi level (Ef) is a very important parameter and can be defined as the electrochemical potential of an electron in a metal or semiconductor, which can be modulated by the applied external potential. In order to promote electrical conduction in a semiconductor, the charge transport should be obtained by one of the following mechanisms: thermal generation, doping, or photoexcitation . Thus, metals and semiconductors are distinguished by the Fermi level position, which is related to the concentration of charge carriers [43–44]. In the n-type semiconductor, the Fermi level is closer to the band conduction, while for the p-type semiconductor it is close to the valence band.
The presence of an essentially filled energy band, a separate almost empty band, leads to semiconductor photosensitivity. The absorption of photons with energy greater than the energy of the "band gap" results in the promotion of electron from the valence band to the conduction band with concomitant generation of a hole (h+) in the valence band. This can be visualized in the Equation (2).
The hole formed on the surface of the catalyst (n-type for instance) can usually promote oxidation of adsorbed species on the semiconductor surface and/or water oxidation leading to the formation of hydroxyl radical, and both can act on organic material degradation. Different mechanisms can be proposed:
The organic matter (OM) from the actinobacteria cell wall, for example, adsorbs on the surface of the photocatalyst and can be oxidized by the holes (h+) in the valence band, forming a cation that can react rapidly with oxygen .
Depending on the chosen semiconductor and the pH of the system, the water adsorbed on the surface is oxidized to hydroxyl radical through the hole from the valence band . As previously mentioned, the hydroxyl radical has a high oxidation power and can promote the oxidation of the species present in the system, subsequently.
The efficiency of photocatalysis depends on the competition between the effectiveness of the electron removal from the semiconductor surface and the recombination process involving electron/hvb+ generating heat as a product [36, 46, 47]:
Therefore, there is high demand for methods that are able to minimize the recombination process of electrons returning from the conduction band to the valence band. Studies reported in the literature have shown that the photocatalytic oxidation can be improved by an anodic bias potential . In the under bias potential, there is a formation of a potential gradient in the interface substrate/electrolyte and the electrons are removed, leading to the decrease in recombination of the pair electron/hole [36, 42]. Figure 3 illustrates the mechanism of PEC.
Understanding the efficient charge separation mechanism in PEC is essential. The moment a semiconductor is in contact with the electrolyte, a junction semiconductor/electrolyte interface is formed in charge of determining the electron hole separation kinetics. Due to the different potential present in the interface, there is a change in the potential Fermi of the semiconductor. Thus, the equilibrium of this interface requires a power flow between the phases, providing the creation of band-bending in the semiconductor phase. The space charge layer (SCL) is the region where there is bending and is characterized by the presence of electrons or holes in the surface [36, 48, 49].
The application of a bias potential also contributes in controlling the Fermi level . Flat band potential is conceptualized as an exact potential for which the potential drops between the surface and the bulk of the electrode is zero. Thus, applying a greater potential than the flat-band potential will provide an increase in band-bending in an n-type semiconductor. In this situation, electrons are depleted and holes are enriched at the surface. The electron that has been excited in the conduction band flows through an external circuit to the counter electrode where reduction reactions may occur such as the reduction of H+ to H2. Figure 4 shows an energy diagram of an n-type (TiO2) semiconductor in different situations: before semiconductor-electrolyte contact, equilibrium established after semiconductor-electrolyte contact, and applying anodic bias.
Thus, the high oxidizing power of hydroxyl radicals formed during photocatalytic and photoelectrocatalytic processes has gained attention in the disinfection process. Their applications in promoting actinobacterium disinfection is reported in the literature and a revision of this contribution is shown in the following sections.
4. Main advanced oxidation process applied to actinobacterium disinfection
Considering the resistance of actinobacterium to conventional disinfection treatments and the promised results of disinfection processes based on advanced oxidation process, the aim of this work is to describe the efficiency of the advanced oxidation process applied to actinobacterium disinfection.
Among the advanced oxidation process applied to actinobacterium disinfection, the main reported are photolysis, photocatalysis, and photoelectrocatalysis specially applied to mycobacteria disinfection. Some of the works related in the literature are show below.
The inactivation by photolysis using mainly ultraviolet (UV) irradiation has been reported by many researches using different UV sources applied specially for
Secondary effluents spiked with
Photocatalytic treatments are based on an irradiation source and a photocatalyst as a semiconductor. Among them, the TiO2 is one of the most powerful semicondutor materials used for photocatalysis due its high activity, strong oxidizing powers, and long-term stability. TiO2 can generate strong oxidizing power when illuminated with UV light at wavelengths lower than 385 nm. The photon energy generates an electron hole pair on the TiO2 surface. The hole in the valence band can then react with water or hydroxide ions adsorbed on the surface to produce hydroxyl radical (⋅OH), and the electron in the conduction band can reduce O2 to produce superoxide ions (O2–). Both holes and ⋅OH are extremely reactive upon contacting organic compounds and microorganisms . However, others semiconductors have been proposed for actinobacterium disinfection and some of the main works are described in this section.
The photocatalysis with immobilized TiO2 and UV irradiation has been proposed as seawater disinfection technology. The method was evaluated using marine bacteria assigned as actinobacteria
The anti-bactericide activity of TiO2 nanofilms deposited onto polyvinyl chloride and glass substrates was evaluated by monitoring
Hetero-nanostructured film of titania nanosheets and lysozyme have been proposed as a semiconductor-like antibacterial agent for
The impregnation of TiO2 with different metals has been proposed to improve the photocatalytic actives, such as Ag, Cu, and Pt. Su et al.  proposed the use of TiO2/Ag nano-antibacterial materials prepared at low temperature using polyethylene glycol (PEG-600) as reducing and stabilizing agents. The antibacterial activity study was carried by growth inhibition rates against
The efficiency of undoped TiO2 and platinized sulfated TiO2 (Pt/TiO2) to photocatalytic oxidation was investigated with microorganisms loaded over photocatalyst films from aerosols to load
The use of Cu-doped TiO2 nanoparticles (NPs) for the inactivation of
Another catalyst that has been reported is Ag/ZnO composite NPs. This photocatalyst was applied for textile treatment. Long-term stable sols of ZnO and Ag/ZnO NPs were prepared and applied as liquid coating agent for textile treatment in combination with an inorganic-organic hybrid polymer binder sols prepared from the precursors 3-glycidyloxypropyltrimethoxysilane (GPTMS) and tetraethoxysilane (TEOS) . The antimicrobial activity of the NPs applied on textile fabrics was tested against the Gram-negative bacterium
The mycobactericidal properties of an iron-based novel heterogeneous-modified polyacrylonitrile (PAN) catalyst in combination with hydrogen peroxide were examined against
There are many photocatalytic actinobacterium disinfection processes based on different semiconductors, mainly TiO2 (pure and impregnate). Although photocatalytic oxidation can be a good option for water disinfection, its performance is greatly restricted by fast electron–hole (e−/h+) recombination. A strategy to increase photocatalytic efficiency is PEC, which consists of introducing a reverse bias potential to the anode coated with the photocatalyst. The PEC process minimizes recombination because the system exists under bias potential, creating a potential gradient on the anode that is enough to remove the electrons from the conduction band to an external counter electrode. This increases the availability of ⋅OH radicals and other reactive oxygen species (ROS) that are able to attack the bacterium cell wall where the bacteria gets in contact with the catalyst. There are few researches about the actinobacteria photoelectrocatalytic inactivation and they are only described for
4.3. Photoelectrocatalysis (PEC)
The photoelectrocatalytic inactivation using TiO2 nanotubular array electrodes of 103 CFU (Colony-Forming Units) mL-1 M
TiO2 nanotubular array electrodes coated with 16% (w/w) Ag NPs (Ti/TiO2-Ag) have shown excellent performance in the disinfection of water containing
The irradiation of Ti/TiO2–Ag with visible irradiation as photoelectrode promoted 99.6% inactivation of
So, among the advanced oxidative process described until this moment, the photoelectrocatalytic treatment gave the best results, since it promotes the inactivation and also degradation of cell lyse components.
4.4. Others alternative advanced oxidation processes
Among the other advanced oxidation processes, we can highlight the use of ozone, Engineered Water Nanostructures, peroxide, and direct electrolysis.
The effect of ozone on cariogenic microorganisms has been reported for actinobacteria
Pyrgiotakis et al.  have been the first to report the use of Engineered Water Nanostructures (EWNS) for mycobacteria inactivation. The method is based on the transformation of atmospheric water vapor into EWNS. Electron paramagnetic resonance (EPR) showed that EWNS contain a large number of ROS, primarily ⋅OH and superoxides.
The disinfection of
Finally, disinfection using electrolyzed strongly acidic water (ESW) against
Then, considering the abundance of the actinobacteria in water mainly due their resistance to conventional water treatment, such as chlorine, the advanced oxidation process is a promising alternative to the water treatment, especially to water used in therapeutic applications.
5. Final consideration
The advanced oxidation process has been reported as an excellent alternative for actinobacterium disinfection. Good results have been obtained by photolysis treatment, however, it requires longer time and there is the possibility of photo-reparation next to a dark period. The use of photocatalysis gave the best results using different photoanodes such as TiO2 (bare and impregnated) with metals such as Au, Ag, and Pt, which can improve the photocatalytic activated. The most promising technique seems to be photoelectrocatalysis as it is able to promote inactivation at a short period of illumination and higher mineralization of products generated from the cellular lyse. Nevertheless, the technique deserves further test to improve the economic aspects involved in using the combination of bias potential and UV irradiation.
The authors thank the financial support from FAPESP, CAPES, and CNPq.