Abstract
This review aims to examine the existence of Pseudomonas aeruginosa (P. aeruginosa) and their antibiotic resistance genes (ARGs) in aquatic settings and the alternative treatment ways. P. aeruginosa in a various aquatic environment have been identified as contaminants with impacts on human health and the environment. P. aeruginosa resistance to multiple antibiotics, such as sulfamethoxazole, ciprofloxacin, quinolone, trimethoprim, tetracycline, vancomycin, as well as specific antibiotic resistance genes including sul1, qnrs, blaVIM, blaTEM, blaCTX, blaAIM-1, tetA, ampC, blaVIM. The development of resistance can occur naturally, through mutations, or via horizontal gene transfer facilitated by sterilizing agents. In addition, an overview of the current knowledge on inactivation of Pseudomonas aeruginosa and ARG and the mechanisms of action of various disinfection processes in water and wastewater (UV chlorine processes, catalytic oxidation, Fenton reaction, and ozonation) is given. An overview of the effects of nanotechnology and the resulting wetlands is also given.
Keywords: Pseudomonas aeruginosa, Antibiotic resistance genes, UV chlorine, Catalytic oxidation, Fenton reaction, Ozonation
List of abbreviations
- UV
Ultra violet
- ARGs
Antibiotic resistance genes
- CF
Cystic fibrosis
- MDR
Multidrug-resistant
- EDNA
Extracellular DNA
- IDNA
Intracellular DNA
- WWTPs
Wastewater treatment plants
- HGT
Horizontal gene transfer
- ABR
Antibiotic resistance bacteria
- MDRPA
Multi-drug-resistant Pseudomonas aeruginosa
- AMSB
Antimicrobial susceptible bacteria
- GIs
Genomic islands
1. Introduction
Our planet, referred to as the "blue planet,” is predominantly covered by water, however, only a small fraction (2.5 %) of this vast resource is freshwater. In light of growing challenges such as changing lifestyles, global water pollution, and declining water quality [1], the critical importance of clean and safe water cannot be overstated. Unfortunately, rapid industrialization, urban expansion, and intensified agricultural practices have led to a surge in toxic wastewater production, posing severe threats to both human health and the environment [2]. Water can harbor a variety of harmful inorganic, organic, and biological pollutants, some of which are carcinogenic [3]. Despite significant advancements in the 20th century, including filtration and chlorination, it is disheartening that more than a billion people worldwide still lack access to clean drinking water [4].
In the 21st century, the challenges in managing water quality have become even more pressing, particularly in densely populated urban areas and regions like the Middle East, where effective water management remains a struggle [5]. The increasing threat of pollutants to water infrastructure is a matter of great concern, as treatment systems often struggle to efficiently remove the contaminants they produce, posing significant health risks to both humans and the environment [6].
Waterborne diseases remain a leading global cause of mortality, with unsafe and contaminated water contributing to hundreds of thousands of deaths, primarily among children [7].
Pseudomonas aeruginosa (P. aeruginosa) is a bacterium that can contaminate various types of water, including drinking water [8]. According to one study, eight isolates of Pseudomonas spp. of the Pseudomonas putida and fluorescent species were found in the consumption water. Therefore, in times of risk, Pseudomonas could participate in the emergence of antibiotic resistance by drinking water [9]. Its ability to form biofilms in plumbing (such as showerheads, faucets, etc.) is more important than its presence in the supply system or drinking water treatment because P. aeruginosa can live in distilled or deionized water [10]. In addition, tap water from hospitals [11]. Bronchoalveolar lavage fluid and water for rinsing in microbiological surveillance [12] Hospital water system [13]. In quantities ranging from 10/100 mL to over 1000/100 mL in natural waters such as lakes and rivers [14]. Water from a rural well [15]. According to the taxonomic designation, Pseudomonas and Legionella were the most detected categories of opportunistic pathogenic bacteria in both treated and untreated rainwater [16]. P. aeruginosa, a Gram-negative bacterium, is widespread across diverse ecological niches in water, soil, and various organisms, including humans [17]. Its multidrug-resistant (MDR) strains are a significant concern in nosocomial infections, including urinary tract infection and severe respiratory particularly affecting individuals with cystic fibrosis (CF), infection in burns, open wounds [18,19]. Foot infection in diabetics and others with poor microvascular circulation; ear infection, particularly otitis externa and chronic suppurative otitis media, which is related with tissue damage and water obstruction; and keratitis, which is associated with prolonged contact lens usage and contaminated contact lenses. Other rare but deadly infections include endocarditis occurring in people with or without injectable drug use, and meningitis linked with penetrating trauma to the head, insertion of a CNS shunt (such as a ventriculoperitoneal (VP) shunt), or post-neurosurgical operations [20,21].
Multidrug resistance has been increased all over the world that is considered a public health threat. Several recent investigations reported the emergence of multidrug-resistant bacterial pathogens from different origins that increase the necessity of the proper use of antibiotics [22]. Besides, the routine application of the antimicrobial susceptibility testing to detect the antibiotic of choice as well as the screening of the emerging MDR strains [23]. The escalating resistance of P. aeruginosa to conventional antibiotics necessitates innovative eradication methods [24].
2. Virulence determinants of P. aeruginosa
2.1. Secretion systems
The Type 1 secretion system (T1SS) transfers the alkaline protease AprA, while the Type 2 secretion system (T2SS) controls the secretion of multiple virulence factors, including exotoxin A (ToxA), proteases LasA and LasB, and the hemolytic phospholipase C (PlcH). The Type 3 secretion system (T3SS) functions as a needle-like nanomachine that delivers toxic effectors – ExoS, ExoT, ExoU, and ExoY – into the target host cell [25]. P. aeruginosa exhibits remarkable survival mechanisms against antimicrobial agents due to essential protein secretion systems, such as the type VI secretion system (T6SS), which playing a role in virulence and antibacterial competition [26]. Furthermore, the functional annotation of hypothetical proteins (HPs) may unveil new targets to enhance P. aeruginosa treatment and investigation [27,28].
3. Significance biofilm formation in P. aeruginosa
The establishment of a microbial biofilm relies on the creation of a matrix consisting of extracellular polymeric molecules that embed the bacteria together into a strong colony. The matrix is composed of three exopolysaccharides (Pel, Psl, and alginate), as well as extracellular DNA and proteins. These bacterial biofilm populations are usually resistant to antibiotic treatment and human immunity [21].
Their contamination potential extends to various water types, including drinking water, with specific Pseudomonas spp. Isolates, such as P. Putida and P. fluorescens, posing a potential risk for antibiotic resistance emergence [8,9]. Biofilm formation, a crucial defense mechanism against antibacterial drugs, is prevalent in aquatic environments, contributing to persistent infections and increased morbidity [29]. P. aeruginosa's adaptability to diverse water sources, its presence in plumbing systems, and its identification in various natural water bodies emphasize the need for effective water management and treatment [[10], [11], [12], [13], [14], [15], [16],30].
4. Antibiogram of P. aeruginosa
P. aeruginosa shows resistance to a range of antibiotics, including aminoglycosides, β-lactams and quinolones. Antibiotic resistance in P. aeruginosa is mostly due to acquired and intrinsic mechanisms, including poor membrane permeability, antibiotic resistance genes, and active efflux pumps. P. aeruginosa's outer membrane proteins (oprL) play an important role in antibiotic and antiseptic resistance. ESBL genes encode extended β-lactamases (ESBLs), which cause resistance to β-lactam antibiotics like penicillin and cephalosporins. The most prevalent ESBL genes associated with P. aeruginosa are blaCTX-M and blaTEM [31].
The widespread contamination of water bodies and the emergence of antibiotic-resistant bacteria have become significant global public health concerns, highlighting the urgency to develop advanced technologies for enhancing wastewater treatment standards [32] (Fig. 1). Antibiotic resistance has escalated to a critical global health issue in the twenty-first century, leading to a decline in the efficacy of antibiotics for treating infections, as recognized by the World Health Organization [33].
Fig. 1.
Types of water contamination of P. aeruginosa.
Antibiotic resistance genes (ARGs) are detected in both extracellular and intracellular DNA (eDNA and iDNA), with eDNA originating from bacterial cell lysis and active secretion from live bacteria [34]. These genes have been found in various aquatic environments, often involving mobile genetic components such as plasmids, integrons, and transposons [35,36]. Human and animal waste is the primary source of antibiotic dissemination into the environment, containing significant amounts of unmetabolized antimicrobials [37]. The widespread use of antibiotics in households results in their presence in wastewater, making municipal wastewater treatment plants (WWTPs) major contributors to ARGs and antibiotic-resistant bacteria (ARB) in the environment [38].
WWTPs have been identified as hotspots for horizontal gene transfer (HGT), enabling the widespread transmission of ARGs and serving as potential storage and ecological reservoirs for antibiotic resistance [39]. Antibiotics’ environmental persistence has been discovered in water resources, with adverse effects on environmental health, impacting microbial structure and development in ecology [[40], [41], [42]]. ARGs are now recognized as environmental pollutants that can spread through human and animal sources, affecting drinking water supplies and natural ecosystems [39,43,44]. Their persistence in streams and rivers is observed even after being released from hospital wastewater treatment plants (HWWTP) [45,46].
To safeguard the aquatic environment and human health, it is imperative to develop innovative methods for assessing the environmental risks associated with the spread both antimicrobial susceptible bacteria (AMSB) and antimicrobial-resistant bacteria (AMRB) in the aquatic environments [47].
This comprehensive review seeks to address a critical concern in water quality management-the presence and persistence of P. aeruginosa, a bacterium recognized by the World Health Organization for its potential threat to human health. We delve into the persistence of P. aeruginosa on hospital surfaces and its alarming resistance to antimicrobial agents. By examining methods to decontaminate water sources from this pathogen, our objective is to provide insights into effective strategies that can safeguard both public health and the environment.
5. Pseudomonas aeruginosa antibiotic resistance genes (ARGs)
P. aeruginosa, a bacterium with increasing antibiotics resistance, is a key concern in hospital wastewaters, identified as a significant source of antibiotics, antibiotic resistant bacteria (ARBs), and ARGs in the environment [48]. Resilient on hospital surfaces, P. aeruginosa contributes to the global presence various ARGs such as sul1, qnrs, blaVIM, blaTEM, blaCTX, blaAIM-1, tetA, ampC, blaVIM [49,50]. The potential for aquatic ecosystems to facilitate the interaction between indigenous bacteria and antibiotic-resistant ones, introduced via wastewater discharges, may lead to the transmission of ARGs to humans and animals through drinking water [51].
Even with disinfection measures in place to inactivate ARBs, a notable proportion of ARGs may persist, raising concerns about their transmission [52]. Vertical transmission plays a crucial role in the dissemination of acquired antibiotic resistance by P. aeruginosa through water [53]. Carbapenems, a vital class of beta-lactams for severe infections, encounter particular challenges with resistance in P. aeruginosa, further complicated by limited global approval for veterinary medicine use [54,55]. The detection of the blaAIM-1 gene for carbapenems resistance in wastewater samples from diverse sources, including healthcare and non-healthcare streams, as well as river water underscores the potential environmental impact [56] (Fig. 2).
Fig. 2.
Main carbapenems and imipenem genes known to be involved in increase P. aeruginosa antibiotic resistance.
The transmission and mobility of acquired genes, especially those encoding carbapenemases, involve various mobile genetic elements like plasmids, integron gene cassettes, transposons, and genomic islands. These components can migrate between genomes, exhibiting both intracellular and intercellular mobility through mechanisms such as transformation, conjugation, and transduction [57].
6. The link between the accessory genome and resistance dissemination in P. aeruginosa
Certain stains of P. aeruginosa, exemplified by Gene, exhibit remarkable adaptability to specific environmental conditions, resulting in the formation of an accessory genome. This genome encompasses a diverse array of genetic elements, including genomic islands (GIs), transposons, integrons, insertion sequences, prophages, plasmids, and integrative and conjugative elements (ICEs). Additionally, the overall genome of PA34 consists of 6.8 Mbp chromosome and two plasmids of 95.4 Kbp (pMKPA34-1) and 26.8 Kbp (pMKPA34-2), collectively encoding 1213 genes that contribute to a sizable auxiliary genome. Notably, these unique genes are associated with various attributes, including phage integrase, transposons, and both metal and antibiotic resistance.
Among the genomic islands (GIs), approximately 24 have been predicted within the entire chromosome, with two integrated into distinct locations. Remarkably, eleven of these GIs either replace pathogenic genes or bear virulence factors. The inclusion of the aminoglycoside resistance gene (AAC (3)-IId) within a bacteriophage highlights the intricate nature of resistance mechanisms in P. aeruginosa [58]. The larger genome size of P. aeruginosa may facilitate horizontal gene transfer (HGT) across diverse organisms due to reduced effects of codon bias. The elevated guanine cytosine (GC) content of P. aeruginosa also contributes to the assimilation of foreign DNA. However, genes and elements acquired through HGT may display a lower GC content due to genetic drift [59].
Emerging evidence suggests that mutational events play a significant role in the development of antibiotic resistance (AR) in P. aeruginosa. The proliferation of mobile genetic elements (MGEs) safeguarding AR genes adds to the complexity of the accessory genome, potentially carrying significant implications for public health [60].
7. Methods of treatment
7.1. Nanotech advances in water treatment: antibacterial impact
Over the last few decades, research in nanomaterial and nanotechnology has yielded a new understanding of fundamental processes and introduced revolutionary breakthroughs across a variety of traditional fields, including wastewater treatment. Nanotechnology is being explored as a potentially useful technology, and it has already shown excellent progress in multiple areas [61]. It is anticipated that the highly modular, multifunctional, and efficient processes of nanotechnology will provide powerful, high-performance, and affordable solutions for water and wastewater treatment [62]. Nanomaterial is generally defined as materials that are smaller than 100 nm in at least one dimension and possess high reactivity, functionalization, a large specific surface area, and size-dependent properties that make them suitable for water purification [63]. Certain nanomaterial can be used as disinfectants due to their antibacterial properties, reducing the risk of toxic disinfection byproducts (DBPs) forming during the typical disinfection process [64]. Various types of metal nanoparticles (NPs) have been found to cause multiple injuries to bacterial cells, such as disintegration of peptidoglycan, rupture of the cell membrane leading to the leakage of intracellular contents, release of reactive oxygen species (ROS) resulting in bacterial cell death, and the harmful effects of heavy metal ion release on cellular components [65]. Research trends indicate a growing interest in exploring nanoparticles to treat antibiotic-resistant bacteria [66]. Additionally, for economic and unspecified health reasons, the nanotechnology is expected to become increasingly important in the treatment of human disease in the near future. Nanoparticles show potential in effectively removing contaminants and bacteria in water treatment [67] (Table 1). The potential applications of lanthanum calcium manganate nanoparticles (LCMO) include their use in antibacterial drugs and water treatment technologies. These nanoparticles, along with other types such as colossal magneto resistance (CMR) and Eu3+doped lanthanum calcium manganate nanoparticles (LECMO), have the ability to efficiently remove pollutants and microbes from water. The synthesized nanoparticles ranged in size from 50 nm to 200 nm and exhibited a single-phase LCMO or LECMO structure with an orthorhombic crystal structure after annealing the precursor at 1000_C for 2 h in the air. Additionally, the antibacterial activity against P. aeruginosa-ATCC 27853 was assessed. The study found that LCMO nanoparticles exhibited superior antibacterial activity compared to LECMO nanoparticles [68]. Cobalt oxide (Co3O4) nanoparticles have diverse applications in engineering, biomedical, and environmental fields. Co3O4 nanoparticles and their nanocomposites are utilized to eliminate antibiotic-resistant bacteria in wastewater [69]. Nano-Ag has become increasingly popular as an antibacterial nanomaterial due to its potent and broad antibacterial activity, safety, and ease of production, making it the preferred material for water decontamination [70]. The release of silver ions from nano-silver in water leads to the binding and damage of SH groups in enzyme systems [71]. The antibacterial effect of Nano-silica silver Nano composite (NSAgNC) was investigated for water disinfection against P. aeruginosa, demonstrating significant antibacterial activity in a dosing strategy, resulting in the elimination of 99 % of P. aeruginosa within 5 h at a concentration of 1.5 mg/mL NSAgNC (5.1 wt% AG). The early binding of NSAgNC to the cell wall damaged cell membrane integrity and led to cytoplasm leakage. The inhibition of respiratory chain dehydrogenase by NSAgNC caused the inactivation of cell metabolism and decreased cell viability [72]. In contrast, iron- and copper-based nanoparticles are anticipated to interact with peroxides in the environment, generating free radicals that are highly toxic to microorganisms. Recently, copper oxide nanoparticles (80–160 nm) were evaluated for their antibacterial activity against P. aeruginosa, Klebsiella pneumonia, Salmonella paratyphoid, and Shigella strains. Additionally, nanoparticles of zinc oxide (ZnO) and magnesium oxide (MgO) are effective in eliminating microorganisms and are currently used as food preservatives [73].
Table 1.
List of nanoparticles and their minimum bactericidal concentration (MBC) against P. aeruginosa.
7.2. Advanced disinfection for waterborne pathogens
Pathogenic microorganisms in water, food, and foam can be effectively eliminated using commonly used disinfectants, including UV and chlorine [77]. Chlorination of drinking water has played a vital role in preventing and controlling waterborne disease epidemics globally [78]. Organic chemicals can undergo various pathways for response, such as electrophilic substitution, addition, and oxidation. The rate constant for chlorination of organic compounds can differ significantly, ranging from less than 0.1 to 109 M−1 s −1. On the other hand, chlorination of inorganic chemicals typically happens through an electrophilic attack of HOCl [79]. UV irradiation uses is another disinfection method that utilizes ultraviolet light to damage the DNA of bacteria, viruses, and other pathogens in water, preventing their replication. UV irradiation and chlorination have been used for a long time to disinfect water. However, the use of either UV irradiation or chlorination exclusively may have limitations, such as the potential for live but non-culturable bacteria production and bacterial reactivation [80]. Various methods have been explored to disinfect drinking water and wastewater, including the use of UV and chlorine. In a study, P. aeruginosa was selected as the target pathogen to test the feasibility of the UV/chlorine method, and it was found that this method significantly reduced metabolic activity and harmful gene levels in the pathogen [81]. Notably, UV/chlorine therapy was more effective in preventing bacterial dark reactivation than UV or chlorination alone. In addition, advanced UV oxidation processes with hydrogen peroxide and UV photolysis are being investigated to extend their reach to the inactivation of DNA-damaged and antibiotic-resistant bacteria in wastewater treatment [82]. Another study showed that exposure to chlorine led to a decrease in P. aeruginosa numbers, but cells acclimated to tap water could no longer be cultured [83]. An ultraviolet (UV)-based advanced oxidation process with hydrogen peroxide and UV radiation was used as a pretreatment method to control biofilms in water. Surviving cells of P. aeruginosa were found to develop an adherent biofilm under UV-based Advance oxidation processes (AOP) therapy, while H2O2/UV could only prevent biofilm formation over long periods in combination with residual H2O2. The potential benefit of AOP was demonstrated when it resulted in better biofilm management than UV-based AOP therapy maintained with comparable amounts of residual H2O2 [84] (Table 2). However, the chlorination process was found to promote the natural horizontal transformation of RP4 plasmids, leading to the exchange of ARGs between P. aeruginosa and the formation of new ARBs, as well as the transfer of chlorine-damaged opportunistic pathogens from non-ARB to ARB [85]. Additionally, a study on the outcome of P. aeruginosa biofilm showed that biofilm extracellular polymeric substances had different effects on biofilm-resistant and detached biofilms on chlorine-based disinfectants, suggesting the importance of understanding the structure and composition of biofilms in developing effective disinfection strategies [86].
Table 2.
Biofilm formation (%) of P. aeruginosa PAO1 after short (<24 h, left) and long (days, right) incubation periods post treatment, using (a) full-UV with 5 mg l-1 H2O2, and filtered-UV (>295 nm) with (b) 5 mg l-1 H2O2 and (c) 1 mg l-1 H2O2. Adapted from Ref. [84].
| (a) Full-UV and 5 mg l−1 H2O2 | 18 h |
3 days |
||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Control | H2O2 | 15s | 30s | 60s | Control | H2O2 | 15s | 30s | 60s | |
| (1) Control | 100-+16 | 100-+4 | 78-+6 | |||||||
| (2) H2O2 5mg1−1 | ||||||||||
| (3) Full-UV | 17-+3 | 34-+3 | 27-+2 | 4-+2 | 84-+5 | 82-+3 | 71-+2 | |||
| (4) Full- UV + OH (catalase) | 40-+8 | 22-+1 | 3-+1 | |||||||
| (5) Full- UV + OH + residual H2O2 | 3-+1 | 3-+1 | 2-+1 | 6-+10 | 7-+13 | 1-+0 | ||||
| (b) Full-UV (>295 nm) and 5 mg l−1 H2O2 | 22 h |
9 days |
||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Control | H2O2 | 5 min | 10 min | 15 min | Control | H2O2 | 5 min | 10 min | 15 min | |
| (1) Control | 100-+19 | 100-+7 | ||||||||
| (2) H2O2 5mg1−1 | 79-+5 | 100 | ||||||||
| (3) Full-UV | 71-+5 | 59-+11 | 60-+5 | 100 | 100 | 100 | ||||
| (4) Full- UV + OH (catalase) | 55-+5 | 34-+2 | 18-+2 | |||||||
| (5) Full- UV + OH + residual H2O2 | 1-+1 | 1-+1 | 0-+0 | 100 | 100 | 2-+2 | ||||
| (c) Full-UV (>295 nm) and 1 mg l−1 H2O2 | 22 h |
9 days |
||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Control | H2O2 | 5 min | 10 min | 15 min | Control | H2O2 | 5 min | 10 min | 15 min | |
| (1) Control | 100-+19 | 100-+7 | ||||||||
| (2) H2O2 5mg1−1 | 87-+4 | 100 | ||||||||
| (3) Full-UV | 71-+5 | 59-+11 | 60-+5 | 100 | 100 | 100 | ||||
| (4) Full- UV + OH (catalase) | 56-+4 | 39-+6 | 38-+11 | |||||||
| (5) Full- UV + OH + residual H2O2 | 65-+8 | 39-+6 | 27-+6 | 100 | 100 | 100 | ||||
7.3. Solar-powered oxidation and ozonation: P. aeruginosa and antibiotic resistance genes
Numerous studies have investigated the efficacy of solar-powered Fenton oxidation and ozonation on P. aeruginosa and ARGs [87]. Since the 1950s, ozone treatment has been used to treat hospital wastewater, and several studies have demonstrated its effectiveness in eliminating a range of pathogens, including P. aeruginosa [88]. Additionally, AOP have been employed to treat water contaminated with diverse pollutants. These techniques are capable of killing microbes due to their potent oxidizing ability and reactivity [68]. The oxidative species, OH, is formed in Fenton reactions by the interaction of Fe2 with H2O2 (Fe2 H2O2/Fe3 OH OH). In Fenton reactions powered by sunlight, the Fe3 created during the reaction is photo-reduced to regenerate the Fe2 (for example, [Fe (H2O)]3+hv/Fe2 H++ OH) [89]. Ozone, as gaseous molecule and allotrope of oxygen, reacts with both inorganic and organic substances, and ozonation is a powerful method for reducing or inactivating microorganisms by generating highly reactive radicals [90]. One mechanism of ozone disinfection involves the disintegration of cell walls, which resulted in the escape of molecules from the cell, and damage to nucleic acids and carbon-nitrogen bonds of proteins [91,92]. The electro-Fenton method was found to be more effective in removing both intracellular and extracellular ARGs of two targets, tetA and ampC, harbored in P. aeruginosa. In the presence of 1.0 mmol/L Fe2, after 120 min of electro-Fenton treatment, the removal efficiency was 3.8 log for intracellular tetA, 4.1 log for intracellular ampC, 5.2 log for extracellular tetA, and 4.8 log for extracellular ampC. This method holds promise for removing intracellular and extracellular ARGs from wastewater [93]. Graywater is wastewater generated from bathtubs, showers, sinks, and kitchen sinks, which does not contain sanitary wastewater. In disinfection experiments, adding hydrogen peroxide (150 mg. L1) to pretreated graywater and exposing it to natural sunlight or artificial sunlight from UV lamps resulted in the complete inactivation of P. aeruginosa [94].
7.4. Advancing photocatalysis and Photodynamic approaches for antibiotic-resistant pathogens
Several research papers have been released discussing the photocatalytic inactivation of antibiotic-resistance genes. Additionally, Photodynamic therapy is an emerging approach to combat the pathogenic diseases [49,95] (Fig. 3). The effectiveness of this therapy can be further improved by utilizing chemical penetration that enhance to bacterial membrane permeability. On study used the cationic photosensitizer toluidine blue O (TBO) to inhibit P. aeruginosa, and found that the presence of TBO (5 g/mL) significantly reduced bacterial growth [96]. Photocatalysis is a highly advanced method for treating wastewater due to its rapid oxidation, lack of byproducts, and ability to oxidize impurities and hydrolysis byproducts at the parts per billion level [97]. whereas the photocatalytic processes is indirect regarding which reactive oxygen species (O2, OH, 1 O2) are generated (e.g., TiO2 + hv + H2O --- O2, OH, 1 O2) [98]. Nanotechnology has also yielded promising water treatment such as photocatalysis, nanofiltration, and nanosorbents [99]. Photocatalysis involves a complex five-phase process that includes reactant diffusion, absorption, reaction, desorption and product diffusion [100], and uses light-active nanostructured catalyst media to degrade various water pollutants. In one study, the photocatalytic activity of titanium dioxide (TiO2) nanoparticles showed significant antibiofilm activity against P. aeruginosa [101,102] and TiO2 photocatalysis was found to reduce the two ARGs, mecA and ampC, in the antibiotic-resistant host bacterium P. aeruginosa [103,104].
Fig. 3.
Photodynamic inactivation of bacteria mediated by eosin Y at different concentrations and irradiated by green LED (5, 10 and 15 min). (a) P. aeruginosa, (b) Escherichia coli, (c) Salmonella Typhimurium, (d) Bacillus cereus and (e) Staphylococcus aureus. Positive control (bacteria and PBS), photosensitizer control (bacteria and eosin Y without light) and light control (bacteria exposed to LED in the absence of photosensitizer). Columns with symbols differ statistically (P < 0·05) (a–c:
positive control;
photosensitizer control;
light control;
0·5 μmol l−1;
5·0 μmol l−1;
10·0 μmol l−1. d:
positive control;
photosensitizer control;
light control;
1·0 μmol l−1;
2·5 μmol l−1;
5·0 μmol l−1;
7·5 μmol l−1. e:
positive control;
photosensitizer control;
light control;
0·1 μmol l−1;
0·25 μmol l−1;
0·5 μmol l−1;
1·0 μmol l−1;
5·0 μmol l−1). Adapted from Ref. [49].
Treatment with TiO2/UVA was found to damage the bacterial membrane and disrupt cell viability and cultivability, as well as suppress the production of virulence factors such as biofilm, protease, and lipase [105]. UVA/TiO2 treatment also eliminated P. aeruginosa's ability to communicate through “quorum sensing” and mobility with swarm types. Heterogeneous photocatalysis using UVA/TiO2 P25 slurry (200 mg L-1 30), UVA/TiO2-immobilised and VA/TiO2-immobilised/H2O2 was also effective in inactivating antibiotic-resistant P. aeruginosa [106]. The photocatalytic activity of CuO/ZnO inhibited the bacterial growth by 1.8 log CFU/mL upon irradiation with visible light [107]. In another study, Bi2WO6/BiVO4 composites were found to have higher photocatalytic antifouling activity than pure Bi2WO6 and BiVO4 when irradiated with visible light and were able to destroy P. aeruginosa after 30 min of [108].
8. Conclusion
In summary, P. aeruginosa is recognized as harmful species responsible for severe diseases in both humans and animals, exhibiting widespread antibiotic resistance and distribution in nature. Therefore, this review aims to compile information concerning the spread of these bacteria and various strategies for their elimination. The presence of ARGs and ARB has been documented in diverse environments, including sewage treatment plants, wastewater, sewage sludge, municipal solid waste, soils, and lakes, rivers, and livestock operations worldwide. P. aeruginosa, naturally found in experimental wastewater, emerges as a promising indicator for wastewater disinfection. However, a research gap persists regarding the efficacy of disinfection methods in real-world drinking water and wastewater treatment plants.
Chemical disinfectants such as chlorine, ozone, and Fenton's reagent demonstrate effectiveness in inactivation P. aeruginosa and ARGs but further understanding is needed regarding their ability to remove ARGs from treated water, especially considering the widespread use of chlorination. While low-dose UV radiation shows limited efficacy against conjugative transmission, high-dose UV irradiation in deactivating P. aeruginosa and ARGs, albeit with some impact on plasmid-mediated transmissions [109]. TiO2 photocatalytic techniques show promise in activating P. aeruginosa and ARGs, although optimization is necessary due to extended treatment durations. Additionally, exploring the role of nanoparticles in wastewater and sewage sludge in influencing ARGs transmission between different genera represents a prospective a venue for research.
In conclusion, this review underscores the widespread presence of ARGs and ARB in various environmental contexts and highlights the potential of P. aeruginosa as an innovative indicator for wastewater disinfection. While certain disinfection approaches exhibit promise, further investigation is crucial for a comprehensive understanding of their effectiveness in mitigating ARG spread. Advancements in UV irradiation, photocatalytic methods and nanoparticle research are pivotal in enhancing our capability to combat antibiotic resistance dissemination in aquatic ecosystems.
Funding
The authors have not received any financial support from funding agencies for this work.
CRediT authorship contribution statement
Alariqi Reem: Writing – review & editing, Writing – original draft, Methodology, Formal analysis, Data curation, Conceptualization. Siham Almansoob: Writing – review & editing, Writing – original draft. Ahmed M. Senan: Writing – review & editing. Aditya Kumar Raj: Writing – review & editing. Rajesh Shah: Writing – review & editing. Mukesh Kumar Shrewastwa: Writing – review & editing. Jay Prakash Prasad Kumal: Writing – review & editing, Writing – original draft, Conceptualization.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Not applicable.
Contributor Information
Alariqi Reem, Email: nasherreem12@gmail.com.
Siham Almansoob, Email: dr.almansoob2010@yahoo.com.
Ahmed M. Senan, Email: 77senan@gmail.com.
Aditya Kumar Raj, Email: adityarajphysio@gmail.com.
Rajesh Shah, Email: hirajeshshah@gmail.com.
Mukesh Kumar Shrewastwa, Email: mshrewastwa55@gmail.com.
Jay Prakash Prasad Kumal, Email: jppkumal@gmail.com.
References
- 1.Chong M.N., et al. Recent developments in photocatalytic water treatment technology: a review. Water Res. 2010;44(10):2997–3027. doi: 10.1016/j.watres.2010.02.039. [DOI] [PubMed] [Google Scholar]
- 2.Qu X., et al. Nanotechnology for a safe and sustainable water supply: enabling integrated water treatment and reuse. Acc. Chem. Res. 2013;46(3):834–843. doi: 10.1021/ar300029v. [DOI] [PubMed] [Google Scholar]
- 3.Ali I. New generation adsorbents for water treatment. Chem Rev. 2012;112(10):5073–5091. doi: 10.1021/cr300133d. [DOI] [PubMed] [Google Scholar]
- 4.Shannon M.A., et al. Science and technology for water purification in the coming decades. Nature. 2008;452(7185):301–310. doi: 10.1038/nature06599. [DOI] [PubMed] [Google Scholar]
- 5.Wang J., Wang S. Microbial degradation of sulfamethoxazole in the environment. Appl. Microbiol. Biotechnol. 2018;102(8):3573–3582. doi: 10.1007/s00253-018-8845-4. [DOI] [PubMed] [Google Scholar]
- 6.Hong Y., et al. Fast-target analysis and hourly Variation of 60 Pharmaceuticals in wastewater using UPLC-high Resolution mass spectrometry. Arch. Environ. Contam. Toxicol. 2015;69(4):525–534. doi: 10.1007/s00244-015-0214-z. [DOI] [PubMed] [Google Scholar]
- 7.WHO Guidelines Approved by the Guidelines Review Committee . Guidelines for Drinking-Water Quality: Fourth Edition Incorporating the First Addendum. World Health Organization; Geneva: 2017. Copyright © World Health Organization 2017. [PubMed] [Google Scholar]
- 8.Hu Y., et al. Risk assessment of antibiotic resistance genes in the drinking water system. Sci. Total Environ. 2021;800 doi: 10.1016/j.scitotenv.2021.149650. [DOI] [PubMed] [Google Scholar]
- 9.Flores Ribeiro A., et al. Occurrence of multi-antibiotic resistant Pseudomonas spp. in drinking water produced from karstic hydrosystems. Sci. Total Environ. 2014;490:370–378. doi: 10.1016/j.scitotenv.2014.05.012. [DOI] [PubMed] [Google Scholar]
- 10.Mena K.D., Gerba C.P. Risk assessment of Pseudomonas aeruginosa in water. Rev. Environ. Contam. Toxicol. 2009;201:71–115. doi: 10.1007/978-1-4419-0032-6_3. [DOI] [PubMed] [Google Scholar]
- 11.Hutchins C.F., et al. Contamination of hospital tap water: the survival and persistence of Pseudomonas aeruginosa on conventional and 'antimicrobial' outlet fittings. J. Hosp. Infect. 2017;97(2):156–161. doi: 10.1016/j.jhin.2017.06.005. [DOI] [PubMed] [Google Scholar]
- 12.Zhang Y., et al. Bronchoscope-related Pseudomonas aeruginosa pseudo-outbreak attributed to contaminated rinse water. Am. J. Infect. Control. 2020;48(1):26–32. doi: 10.1016/j.ajic.2019.06.013. [DOI] [PubMed] [Google Scholar]
- 13.Walker J., Moore G. Pseudomonas aeruginosa in hospital water systems: biofilms, guidelines, and practicalities. J. Hosp. Infect. 2015;89(4):324–327. doi: 10.1016/j.jhin.2014.11.019. [DOI] [PubMed] [Google Scholar]
- 14.Jia F., et al. A low-Field magnetic Resonance Imaging Aptasensor for the rapid and Visual sensing of Pseudomonas aeruginosa in food, Juice, and water. Anal. Chem. 2021;93(24):8631–8637. doi: 10.1021/acs.analchem.1c01669. [DOI] [PubMed] [Google Scholar]
- 15.Wang S., et al. [Molecular epidemiology of drug resistance genes and carbapenem resistance of Pseudomonas aeruginosa in rural well water] Zhonghua Liuxingbingxue Zazhi. 2021;42(5):898–902. doi: 10.3760/cma.j.cn112338-20200904-01127. [DOI] [PubMed] [Google Scholar]
- 16.Reyneke B., et al. EMA-amplicon-based sequencing informs risk assessment analysis of water treatment systems. Sci. Total Environ. 2020;743 doi: 10.1016/j.scitotenv.2020.140717. [DOI] [PubMed] [Google Scholar]
- 17.Toval F., et al. Predominance of carbapenem-resistant Pseudomonas aeruginosa isolates carrying blaIMP and blaVIM metallo-β-lactamases in a major hospital in Costa Rica. J. Med. Microbiol. 2015;64(Pt 1):37–43. doi: 10.1099/jmm.0.081802-0. [DOI] [PubMed] [Google Scholar]
- 18.Caselli D., et al. Multidrug resistant Pseudomonas aeruginosa infection in children undergoing chemotherapy and hematopoietic stem cell transplantation. Haematologica. 2010;95(9):1612–1615. doi: 10.3324/haematol.2009.020867. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Lund-Palau H., et al. Pseudomonas aeruginosa infection in cystic fibrosis: pathophysiological mechanisms and therapeutic approaches. Expert Rev Respir Med. 2016;10(6):685–697. doi: 10.1080/17476348.2016.1177460. [DOI] [PubMed] [Google Scholar]
- 20.Venkatesan A., et al. Pseudomonas aeruginosa infective endocarditis presenting as bacterial meningitis. J. Infect. 2005;51(4):e199–e202. doi: 10.1016/j.jinf.2005.02.019. [DOI] [PubMed] [Google Scholar]
- 21.Algammal A.M., et al. oprL gene sequencing, resistance Patterns, virulence genes, quorum sensing and antibiotic resistance genes of XDR Pseudomonas aeruginosa isolated from Broiler Chickens. Infect. Drug Resist. 2023;16:853–867. doi: 10.2147/IDR.S401473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Algammal A.M., et al. Newly Emerging MDR B. cereus in Mugil seheli as the First Report Commonly Harbor nhe, hbl, cytK, and pc-plc Virulence Genes and bla1, bla2, tetA, and ermA Resistance Genes. Infect. Drug Resist. 2022;15:2167–2185. doi: 10.2147/IDR.S365254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Al-Kadmy I.M.S., et al. The secrets of environmental Pseudomonas aeruginosa in slaughterhouses: Antibiogram profile, virulence, and antibiotic resistance genes. Folia Microbiol (Praha) 2023 doi: 10.1007/s12223-023-01116-1. [DOI] [PubMed] [Google Scholar]
- 24.Pöthig A., et al. Antimicrobial activity and Cytotoxicity of Ag(I) and Au(I) Pillarplexes. Front. Chem. 2018;6:584. doi: 10.3389/fchem.2018.00584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Elsen S., et al. A type III secretion negative clinical strain of Pseudomonas aeruginosa employs a two-partner secreted exolysin to induce hemorrhagic pneumonia. Cell host & microbe. 2014;15(2):164–176. doi: 10.1016/j.chom.2014.01.003. [DOI] [PubMed] [Google Scholar]
- 26.Coulthurst S.J. The Type VI secretion system - a widespread and versatile cell targeting system. Res. Microbiol. 2013;164(6):640–654. doi: 10.1016/j.resmic.2013.03.017. [DOI] [PubMed] [Google Scholar]
- 27.Reem A., et al. Functional annotation of hypothetical proteins related to antibiotic resistance in Pseudomonas aeruginosa PA01. Clin. Lab. 2021;67(8) doi: 10.7754/Clin.Lab.2021.210536. [DOI] [PubMed] [Google Scholar]
- 28.Reem A., et al. Functional and structural annotation of a hypothetical protein (PA2373) from Pseudomonas aeruginosa PA01. Int. J. Pharmacol. 2021;17(5):262–270. [Google Scholar]
- 29.Al-Wrafy F.A., et al. Pseudomonas aeruginosa behaviour in polymicrobial communities: the competitive and cooperative interactions conducting to the exacerbation of infections. Microbiol. Res. 2023;268 doi: 10.1016/j.micres.2022.127298. [DOI] [PubMed] [Google Scholar]
- 30.Teodoro A., et al. Alternative use of Pseudomonas aeruginosa as indicator for greywater disinfection. Water Sci. Technol. 2018;78(5–6):1361–1369. doi: 10.2166/wst.2018.408. [DOI] [PubMed] [Google Scholar]
- 31.Elbehiry A., et al. Pseudomonas species prevalence, protein analysis, and antibiotic resistance: an evolving public health challenge. Amb. Express. 2022;12(1):53. doi: 10.1186/s13568-022-01390-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Karkman A., et al. Antibiotic-resistance genes in waste water. Trends Microbiol. 2018;26(3):220–228. doi: 10.1016/j.tim.2017.09.005. [DOI] [PubMed] [Google Scholar]
- 33.Jałowiecki Ł., et al. Seasonal and technological Shifts of the WHO Priority multi-resistant pathogens in municipal wastewater treatment plant and its receiving surface water: a Case study. Int J Environ Res Public Health. 2021;19(1) doi: 10.3390/ijerph19010336. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Zarei-Baygi A., Smith A.L. Intracellular versus extracellular antibiotic resistance genes in the environment: prevalence, horizontal transfer, and mitigation strategies. Bioresour. Technol. 2021;319 doi: 10.1016/j.biortech.2020.124181. [DOI] [PubMed] [Google Scholar]
- 35.Leonard A.F., et al. Human recreational exposure to antibiotic resistant bacteria in coastal bathing waters. Environ. Int. 2015;82:92–100. doi: 10.1016/j.envint.2015.02.013. [DOI] [PubMed] [Google Scholar]
- 36.Sharma V.K., et al. A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere. 2016;150:702–714. doi: 10.1016/j.chemosphere.2015.12.084. [DOI] [PubMed] [Google Scholar]
- 37.Martínez J.L. Antibiotics and antibiotic resistance genes in natural environments. Science. 2008;321(5887):365–367. doi: 10.1126/science.1159483. [DOI] [PubMed] [Google Scholar]
- 38.Rizzo L., et al. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 2013;447:345–360. doi: 10.1016/j.scitotenv.2013.01.032. [DOI] [PubMed] [Google Scholar]
- 39.Berendonk T.U., et al. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 2015;13(5):310–317. doi: 10.1038/nrmicro3439. [DOI] [PubMed] [Google Scholar]
- 40.Luo Y., et al. A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci. Total Environ. 2014;473–474:619–641. doi: 10.1016/j.scitotenv.2013.12.065. [DOI] [PubMed] [Google Scholar]
- 41.Rosi-Marshall E.J., Kelly J.J. Antibiotic stewardship should consider environmental fate of antibiotics. Environ. Sci. Technol. 2015;49(9):5257–5258. doi: 10.1021/acs.est.5b01519. [DOI] [PubMed] [Google Scholar]
- 42.Willyard C. The drug-resistant bacteria that pose the greatest health threats. Nature. 2017;543(7643):15. doi: 10.1038/nature.2017.21550. [DOI] [PubMed] [Google Scholar]
- 43.Gillings M.R., et al. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. Isme j. 2015;9(6):1269–1279. doi: 10.1038/ismej.2014.226. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Storteboom H., et al. Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environ. Sci. Technol. 2010;44(6):1947–1953. doi: 10.1021/es902893f. [DOI] [PubMed] [Google Scholar]
- 45.Magalhães M.J., et al. Multidrug resistant Pseudomonas aeruginosa survey in a stream receiving effluents from ineffective wastewater hospital plants. BMC Microbiol. 2016;16(1):193. doi: 10.1186/s12866-016-0798-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Nabizadeh Nodehi R., et al. Novel application of in vitro disinfection for modeling the biofilm formation inhibition, antimicrobial susceptibility and antibiotic resistance of Pseudomonas aeruginosa: a study of free and combined chlorine compounds. J Environ Health Sci Eng. 2022;20(1):167–180. doi: 10.1007/s40201-021-00764-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Azuma T., Usui M., Hayashi T. Inactivation of antibiotic-resistant bacteria in wastewater by ozone-based advanced water treatment processes. Antibiotics (Basel) 2022;11(2) doi: 10.3390/antibiotics11020210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Lamba M., Graham D.W., Ahammad S.Z. Hospital wastewater releases of carbapenem-resistance pathogens and genes in urban India. Environ. Sci. Technol. 2017;51(23):13906–13912. doi: 10.1021/acs.est.7b03380. [DOI] [PubMed] [Google Scholar]
- 49.Bonin E., et al. Photodynamic inactivation of foodborne bacteria by eosin Y. J. Appl. Microbiol. 2018;124(6):1617–1628. doi: 10.1111/jam.13727. [DOI] [PubMed] [Google Scholar]
- 50.Szekeres E., et al. Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environ Pollut. 2017;225:304–315. doi: 10.1016/j.envpol.2017.01.054. [DOI] [PubMed] [Google Scholar]
- 51.Anyanwu M.U., Jaja I.F., Nwobi O.C. Occurrence and Characteristics of mobile Colistin resistance (mcr) gene-containing isolates from the environment: a review. Int J Environ Res Public Health. 2020;17(3) doi: 10.3390/ijerph17031028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Dodd M.C. Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J. Environ. Monit. 2012;14(7):1754–1771. doi: 10.1039/c2em00006g. [DOI] [PubMed] [Google Scholar]
- 53.Vaz-Moreira I., Nunes O.C., Manaia C.M. Diversity and antibiotic resistance in Pseudomonas spp. from drinking water. Sci. Total Environ. 2012;426:366–374. doi: 10.1016/j.scitotenv.2012.03.046. [DOI] [PubMed] [Google Scholar]
- 54.Manenzhe R.I., et al. The spread of carbapenemase-producing bacteria in Africa: a systematic review. J. Antimicrob. Chemother. 2015;70(1):23–40. doi: 10.1093/jac/dku356. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Neyestanaki D.K., et al. Determination of extended spectrum beta-lactamases, metallo-beta-lactamases and AmpC-beta-lactamases among carbapenem resistant Pseudomonas aeruginosa isolated from burn patients. Burns. 2014;40(8):1556–1561. doi: 10.1016/j.burns.2014.02.010. [DOI] [PubMed] [Google Scholar]
- 56.Amsalu A., et al. Worldwide distribution and environmental origin of the Adelaide imipenemase (AIM-1), a potent carbapenemase in Pseudomonas aeruginosa. Microb. Genom. 2021;7(12) doi: 10.1099/mgen.0.000715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Yoon E.J., Jeong S.H. Mobile carbapenemase genes in Pseudomonas aeruginosa. Front. Microbiol. 2021;12 doi: 10.3389/fmicb.2021.614058. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Subedi D., et al. Accessory genome of the multi-drug resistant ocular isolate of Pseudomonas aeruginosa PA34. PLoS One. 2019;14(4) doi: 10.1371/journal.pone.0215038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Kung V.L., Ozer E.A., Hauser A.R. The accessory genome of Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 2010;74(4):621–641. doi: 10.1128/MMBR.00027-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60.Botelho J., Grosso F., Peixe L. Antibiotic resistance in Pseudomonas aeruginosa - mechanisms, epidemiology and evolution. Drug Resist Updat. 2019;44 doi: 10.1016/j.drup.2019.07.002. [DOI] [PubMed] [Google Scholar]
- 61.Mapara N., et al. Antimicrobial potentials of Helicteres isora silver nanoparticles against extensively drug-resistant (XDR) clinical isolates of Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 2015;99(24):10655–10667. doi: 10.1007/s00253-015-6938-x. [DOI] [PubMed] [Google Scholar]
- 62.De La Cueva Bueno P., et al. Nanotechnology for sustainable wastewater treatment and use for agricultural production: a comparative long-term study. Water Res. 2017;110:66–73. doi: 10.1016/j.watres.2016.11.060. [DOI] [PubMed] [Google Scholar]
- 63.Ashokkumar M., et al. Editorial to surface tailored innovative materials and technologies for wastewater treatment. Environ Pollut. 2021;284 doi: 10.1016/j.envpol.2021.117436. [DOI] [PubMed] [Google Scholar]
- 64.Hossain F., et al. Antimicrobial nanomaterials as water disinfectant: applications, limitations and future perspectives. Sci. Total Environ. 2014;466–467:1047–1059. doi: 10.1016/j.scitotenv.2013.08.009. [DOI] [PubMed] [Google Scholar]
- 65.Al-Wrafy F.A., et al. Nanoparticles approach to eradicate bacterial biofilm-related infections: a critical review. Chemosphere. 2022;288(Pt 2) doi: 10.1016/j.chemosphere.2021.132603. [DOI] [PubMed] [Google Scholar]
- 66.Ansari M.A., et al. Green synthesis of Al2O3 nanoparticles and their bactericidal potential against clinical isolates of multi-drug resistant Pseudomonas aeruginosa. World J. Microbiol. Biotechnol. 2015;31(1):153–164. doi: 10.1007/s11274-014-1757-2. [DOI] [PubMed] [Google Scholar]
- 67.Lee B., et al. A carbon nanotube wall membrane for water treatment. Nat. Commun. 2015;6:7109. doi: 10.1038/ncomms8109. [DOI] [PubMed] [Google Scholar]
- 68.De D., et al. Antibacterial effect of lanthanum calcium manganate (La0.67Ca0.33MnO3) nanoparticles against Pseudomonas aeruginosa ATCC 27853. J. Biomed. Nanotechnol. 2010;6(2):138–144. doi: 10.1166/jbn.2010.1113. [DOI] [PubMed] [Google Scholar]
- 69.Anele A., Obare S., Wei J. Recent trends and Advances of Co(3)O(4) nanoparticles in environmental Remediation of bacteria in wastewater. Nanomaterials. 2022;12(7) doi: 10.3390/nano12071129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Xu L., et al. Silver nanoparticles: synthesis, medical applications and biosafety. Theranostics. 2020;10(20):8996–9031. doi: 10.7150/thno.45413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71.Valdez-Salas B., et al. Structure-activity relationship of diameter controlled Ag@Cu nanoparticles in broad-spectrum antibacterial mechanism. Mater Sci Eng C Mater Biol Appl. 2021;119 doi: 10.1016/j.msec.2020.111501. [DOI] [PubMed] [Google Scholar]
- 72.Parandhaman T., et al. Antimicrobial behavior of biosynthesized silica-silver nanocomposite for water disinfection: a mechanistic perspective. J. Hazard Mater. 2015;290:117–126. doi: 10.1016/j.jhazmat.2015.02.061. [DOI] [PubMed] [Google Scholar]
- 73.Zhao C., et al. Highly antifouling and antibacterial performance of poly (vinylidene fluoride) ultrafiltration membranes blending with copper oxide and graphene oxide nanofillers for effective wastewater treatment. J. Colloid Interface Sci. 2017;505:341–351. doi: 10.1016/j.jcis.2017.05.074. [DOI] [PubMed] [Google Scholar]
- 74.Jing A.N., De-song W., Xiao-yan Y. Synthesis of stable silver nanoparticles with antimicrobial activities in room-temperature ionic liquids. Chem. Res. Chin. Univ. 2009;25(4):421–425. [Google Scholar]
- 75.Ren G., et al. Characterisation of copper oxide nanoparticles for antimicrobial applications. Int. J. Antimicrob. Agents. 2009;33(6):587–590. doi: 10.1016/j.ijantimicag.2008.12.004. [DOI] [PubMed] [Google Scholar]
- 76.Desai V.S., Meenal K. Antimicrobial activity of titanium dioxide nanoparticles synthesized by sol-gel technique. Res. J. Microbiol. 2009;4(3):97–103. [Google Scholar]
- 77.Chiang E.L.C., et al. Assessment of physiological responses of bacteria to chlorine and UV disinfection using a plate count method, flow cytometry and viability PCR. J. Appl. Microbiol. 2022;132(3):1788–1801. doi: 10.1111/jam.15325. [DOI] [PubMed] [Google Scholar]
- 78.Song Y., et al. Resistance and resilience of representative low nucleic acid-content bacteria to free chlorine exposure. J. Hazard Mater. 2019;365:270–279. doi: 10.1016/j.jhazmat.2018.10.080. [DOI] [PubMed] [Google Scholar]
- 79.Sharma V.K., et al. Organic-coated silver nanoparticles in biological and environmental conditions: fate, stability and toxicity. Adv. Colloid Interface Sci. 2014;204:15–34. doi: 10.1016/j.cis.2013.12.002. [DOI] [PubMed] [Google Scholar]
- 80.Mounaouer B., Abdennaceur H. Modeling and kinetic characterization of wastewater disinfection using chlorine and UV irradiation. Environ. Sci. Pollut. Res. Int. 2016;23(19):19861–19875. doi: 10.1007/s11356-016-7173-4. [DOI] [PubMed] [Google Scholar]
- 81.Wang L., et al. Assessment of the UV/chlorine process in the disinfection of Pseudomonas aeruginosa: efficiency and mechanism. Environ. Sci. Technol. 2021;55(13):9221–9230. doi: 10.1021/acs.est.1c00645. [DOI] [PubMed] [Google Scholar]
- 82.Wang H., et al. Synergistic effect of UV/chlorine in bacterial inactivation, resistance gene removal, and gene conjugative transfer blocking. Water Res. 2020;185 doi: 10.1016/j.watres.2020.116290. [DOI] [PubMed] [Google Scholar]
- 83.Bommer A., et al. Effect of chlorine on cultivability of Shiga toxin producing Escherichia coli (STEC) and β-lactamase genes carrying E. coli and Pseudomonas aeruginosa. Int J Med Microbiol. 2018;308(8):1105–1112. doi: 10.1016/j.ijmm.2018.09.004. [DOI] [PubMed] [Google Scholar]
- 84.Lakretz A., Ron E.Z., Mamane H. Biofilm control in water by a UV-based advanced oxidation process. Biofouling. 2011;27(3):295–307. doi: 10.1080/08927014.2011.561923. [DOI] [PubMed] [Google Scholar]
- 85.Jin M., et al. Chlorine disinfection promotes the exchange of antibiotic resistance genes across bacterial genera by natural transformation. Isme j. 2020;14(7):1847–1856. doi: 10.1038/s41396-020-0656-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 86.Xue Z., et al. Multiple roles of extracellular polymeric substances on resistance of biofilm and detached clusters. Environ. Sci. Technol. 2012;46(24):13212–13219. doi: 10.1021/es3031165. [DOI] [PubMed] [Google Scholar]
- 87.Cengiz M., Uslu M.O., Balcioglu I. Treatment of E. coli HB101 and the tetM gene by Fenton's reagent and ozone in cow manure. J Environ Manage. 2010;91(12):2590–2593. doi: 10.1016/j.jenvman.2010.07.005. [DOI] [PubMed] [Google Scholar]
- 88.Svebrant S., et al. On-site Pilot testing of hospital wastewater ozonation to reduce pharmaceutical Residues and antibiotic-resistant bacteria. Antibiotics (Basel) 2021;10(6) doi: 10.3390/antibiotics10060684. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 89.Pliego G., et al. Trends in the intensification of the Fenton process for wastewater treatment: an overview. Crit. Rev. Environ. Sci. Technol. 2015;45(24):2611–2692. [Google Scholar]
- 90.Shu Z., et al. Pilot-scale UV/H2O2 advanced oxidation process for municipal reuse water: assessing micropollutant degradation and estrogenic impacts on goldfish (Carassius auratus L.) Water Res. 2016;101:157–166. doi: 10.1016/j.watres.2016.05.079. [DOI] [PubMed] [Google Scholar]
- 91.Hocquet D., Muller A., Bertrand X. What happens in hospitals does not stay in hospitals: antibiotic-resistant bacteria in hospital wastewater systems. J. Hosp. Infect. 2016;93(4):395–402. doi: 10.1016/j.jhin.2016.01.010. [DOI] [PubMed] [Google Scholar]
- 92.Hou J., et al. Simultaneous removal of antibiotics and antibiotic resistance genes from pharmaceutical wastewater using the combinations of up-flow anaerobic sludge bed, anoxic-oxic tank, and advanced oxidation technologies. Water Res. 2019;159:511–520. doi: 10.1016/j.watres.2019.05.034. [DOI] [PubMed] [Google Scholar]
- 93.Chen L., et al. Inactivation of antibiotic-resistant bacteria and antibiotic resistance genes by electrochemical oxidation/electro-Fenton process. Water Sci. Technol. 2020;81(10):2221–2231. doi: 10.2166/wst.2020.282. [DOI] [PubMed] [Google Scholar]
- 94.Bajpai M., Katoch S.S., Chaturvedi N.K. Comparative study on decentralized treatment technologies for sewage and graywater reuse - a review. Water Sci. Technol. 2019;80(11):2091–2106. doi: 10.2166/wst.2020.039. [DOI] [PubMed] [Google Scholar]
- 95.Rizzo L., Fiorentino A., Anselmo A. Advanced treatment of urban wastewater by UV radiation: effect on antibiotics and antibiotic-resistant E. coli strains. Chemosphere. 2013;92(2):171–176. doi: 10.1016/j.chemosphere.2013.03.021. [DOI] [PubMed] [Google Scholar]
- 96.Rout B., Liu C.H., Wu W.C. Enhancement of photodynamic inactivation against Pseudomonas aeruginosa by a nano-carrier approach. Colloids Surf. B Biointerfaces. 2016;140:472–480. doi: 10.1016/j.colsurfb.2016.01.002. [DOI] [PubMed] [Google Scholar]
- 97.Chen T., et al. Study on the photocatalytic degradation of methyl orange in water using Ag/ZnO as catalyst by liquid chromatography electrospray ionization ion-trap mass spectrometry. J. Am. Soc. Mass Spectrom. 2008;19(7):997–1003. doi: 10.1016/j.jasms.2008.03.008. [DOI] [PubMed] [Google Scholar]
- 98.Etacheri V., et al. Visible-light activation of TiO2 photocatalysts: Advances in theory and experiments. J. Photochem. Photobiol. C Photochem. Rev. 2015;25:1–29. [Google Scholar]
- 99.Naresh Yadav D., Anand Kishore K., Saroj D. A Study on removal of Methylene Blue dye by photo catalysis integrated with nanofiltration using statistical and experimental approaches. Environ. Technol. 2021;42(19):2968–2981. doi: 10.1080/09593330.2020.1720303. [DOI] [PubMed] [Google Scholar]
- 100.Chen F., et al. The role of Polarization in photocatalysis. Angew Chem. Int. Ed. Engl. 2019;58(30):10061–10073. doi: 10.1002/anie.201901361. [DOI] [PubMed] [Google Scholar]
- 101.Sai Saraswathi V., et al. Biofilm inhibition formation of clinical strains of Pseudomonas aeruginosa mutans, photocatalytic activity of azo dye and GC-MS analysis of leaves of Lagerstroemia speciosa. J. Photochem. Photobiol., B. 2017;169:148–160. doi: 10.1016/j.jphotobiol.2017.03.007. [DOI] [PubMed] [Google Scholar]
- 102.Ansari M.A., et al. Synthesis of Electrospun TiO(2) Nanofibers and characterization of their antibacterial and antibiofilm potential against Gram-positive and Gram-negative bacteria. Antibiotics (Basel) 2020;9(9) doi: 10.3390/antibiotics9090572. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 103.Guo C., et al. H(2)O(2) and/or TiO(2) photocatalysis under UV irradiation for the removal of antibiotic resistant bacteria and their antibiotic resistance genes. J. Hazard Mater. 2017;323(Pt B):710–718. doi: 10.1016/j.jhazmat.2016.10.041. [DOI] [PubMed] [Google Scholar]
- 104.Felis E., et al. Solar-light driven photodegradation of antimicrobials, their transformation by-products and antibiotic resistance determinants in treated wastewater. Sci. Total Environ. 2022;836 doi: 10.1016/j.scitotenv.2022.155447. [DOI] [PubMed] [Google Scholar]
- 105.Achouri F., et al. Effect of photocatalysis (TiO(2)/UV(A)) on the inactivation and inhibition of Pseudomonas aeruginosa virulence factors expression. Environ. Technol. 2021;42(27):4237–4246. doi: 10.1080/09593330.2020.1751729. [DOI] [PubMed] [Google Scholar]
- 106.Jiménez-Tototzintle M., et al. Removal of contaminants of emerging concern (CECs) and antibiotic resistant bacteria in urban wastewater using UVA/TiO(2)/H(2)O(2) photocatalysis. Chemosphere. 2018;210:449–457. doi: 10.1016/j.chemosphere.2018.07.036. [DOI] [PubMed] [Google Scholar]
- 107.Manoharan R.K., et al. Antibacterial and photocatalytic activities of 5-nitroindole capped bimetal nanoparticles against multidrug resistant bacteria. Colloids Surf. B Biointerfaces. 2020;188 doi: 10.1016/j.colsurfb.2020.110825. [DOI] [PubMed] [Google Scholar]
- 108.Ju P., et al. Controllable one-pot synthesis of a nest-like Bi2WO6/BiVO4 composite with enhanced photocatalytic antifouling performance under visible light irradiation. Dalton Trans. 2016;45(11):4588–4602. doi: 10.1039/c6dt00118a. [DOI] [PubMed] [Google Scholar]
- 109.Espinosa-Barrera P.A., et al. Systematic analysis of the scientific-technological production on the use of the UV, H(2)O(2), and/or Cl(2) systems in the elimination of bacteria and associated antibiotic resistance genes. Environ. Sci. Pollut. Res. Int. 2024;31(5):6782–6814. doi: 10.1007/s11356-023-31435-2. [DOI] [PMC free article] [PubMed] [Google Scholar]



