
==== Front
Heliyon
Heliyon
Heliyon
2405-8440
Elsevier

S2405-8440(24)12345-6
10.1016/j.heliyon.2024.e36314
e36314
Review Article
The arsenic bioremediation using genetically engineered microbial strains on aquatic environments: An updated overview
Naiel Mohammed A.E. mohammednaiel.1984@gmail.com
mnaiel@zu.edu.eg
a⁎
Taher Ehab S. b
Rashed Fatema b
Ghazanfar Shakira c
Shehata Abdelrazeq M. d
Mohammed Nourelhuda A. e
Pascalau Raul f
Smuleac Laura laurasmuleac@usvt.ro
g⁎⁎
Ibrahim Ateya Megahed a.eleglany@psau.edu.sa
hi∗∗∗
Abdeen Ahmed jl
Shukry Mustafa k
a Animal Production Department, Faculty of Agriculture, Zagazig University, Zagazig, 44519, Egypt
b Department of Basic Medical and Dental Sciences, Faculty of Dentistry, Zarqa University, Zarqa, 13110, Jordan
c National Institute for Genomics Advanced Biotechnology, National Agricultural Research Centre, Park Road, Islamabad, 45500, Pakistan
d Department of Animal Production, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt
e Department of Physiology and Biochemistry, Faculty of Medicine, Mutah University, Mutah, 61710, Al-Karak, Jordan
f Department of Agricultural Technologies, Faculty of Agriculture, University of Life Sciences "King Mihai I" from Timisoara, Romania
g Department of Sustainable Development and Environmental Engineering Faculty of Agriculture, University of Life Sciences "King Mihai I" from Timisoara, Timisoara, Roman, Romania
h Department of Administration and Nursing Education, College of Nursing, Prince Sattam bin Abdulaziz University, Al-Kharj, 11942, Saudi Arabia
i Department of Family and Community Health Nursing, Faculty of Nursing, Port-Said University, Egypt
j Department of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Benha University, Toukh, 13736, Egypt
k Department of Physiology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, 33516, Egypt
l Department of Biochemistry, Faculty of Veterinary Medicine, South Valley University, Qena, 83523, Egypt
⁎ Corresponding author. mohammednaiel.1984@gmail.commnaiel@zu.edu.eg
⁎⁎ Corresponding author. laurasmuleac@usvt.ro
∗∗∗ Corresponding author. Department of Administration and Nursing Education, College of Nursing, Prince Sattam bin Abdulaziz University, Al-Kharj, 11942,Saudi Arabia. a.eleglany@psau.edu.sa
22 8 2024
15 9 2024
22 8 2024
10 17 e3631419 2 2024
1 8 2024
13 8 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Heavy metal contamination threatens the aquatic environment and human health. Different physical and chemical procedures have been adopted in many regions; however, their adoption is usually limited since they take longer time, are more expensive, and are ineffective in polluted areas with high heavy metal contents. Thus, biological remediation is considered a suitable applicable method for treating contaminates due to its aquatic-friendly features. Bacteria possess an active metabolism that enables them to thrive and develop in highly contaminated water bodies with arsenic (As). They achieve this by utilizing their genetic structure to selectively target As and deactivate its toxic influences. Therefore, this review extensively inspects the bacterial reactions and interactions with As. In addition, this literature demonstrated the potential of certain genetically engineered bacterial strains to upregulate the expression and activity of specific genes associated with As detoxification. The As resistant mechanisms in bacteria exhibit significant variation depending on the genetics and type of the bacterium, which is strongly affected by the physical water criteria of their surrounding aquatic environment. Moreover, this literature has attempted to establish scientific connections between existing knowledge and suggested sustainable methods for removing As from aquatic bodies by utilizing genetically engineered bacterial strains. We shall outline the primary techniques employed by bacteria to bioremediate As from aquatic environments. Additionally, we will define the primary obstacles that face the wide application of genetically modified bacterial strains for As bioremediation in open water bodies. This review can serve as a target for future studies aiming to implement real-time bioremediation techniques. In addition, potential synergies between the bioremediation technology and other techniques are suggested, which can be employed for As bioremediation.

Keywords

Arsenic
Bioremediation
Biotechnology
Contaminant removal
Genome
==== Body
pmc1 Introduction

Heavy metal contamination threatens the aquatic environment and human health [1,2]. Numerous heavy metals such as chromium (Cr), lead (Pb), zinc (Zn), arsenic (As), copper (Cu), cadmium (Cd), nickel (Ni) and mercury (Hg) are the main cause of the contamination of surface and/or groundwater [3]. The aquatic environment might be polluted through septic systems, waste from storage tanks, landfills, hazardous waste sites, pesticides and the application of fertilizers [4,5]. It is recognized that arsenic (As) is a particularly hazardous element in aquatic environments, particularly in its inorganic chemical structure form [6]. The oxidation of sulfide-rich arsenopyrite rocks results in As-containing acid mine drainage, which is a major by-product of the mining of coal, with a total As content exceeding 20 mg L−1 [7]. The discharge of arsenopyrite into the aquatic environment generates two primary forms of As (trivalent arsenite, As III, and pentavalent arsenite, As V) [8]. Specifically, As III is the major chemical form of arsenic pollutants of drainage from acid mines with severe environmental consequences (such as, weathering of bedrock, arsenopyrite oxidation and chief sulfides in rocks, the mine water and surface water mixture, leaching of the arsenic alkali residue, and adsorption-desorption from iron/manganese oxide/hydroxide), and it might be changed into a less hazardous form (As V) in an aerobic condition [9]. As III has a notable negative impact on aquatic organisms due to its weak binding to mineral surfaces. The weak binding is a result of As III being electrically neutral, unlike the negatively charged As (V) oxyanions [10]. Meanwhile, acute or chronic As exposures cause negative health consequences such as cardiovascular disorders, cancer threats, or even sudden death at lethal concentrations [11]. Therefore, the World Health Organization (WHO) has recognized a high permissible level of 10 μg/L for As in drinking water [12]. A recent study discovered that 61 out of 64 districts have higher arsenic levels in their drinking water that exceed the recommended limit set by the World Health Organization (10 μg/L) [13]. This is a significant issue affecting over 85 million people. It is worth noting that shallow groundwater in sedimentary lacustrine aquifers tends to have higher arsenic levels, whereas deeper aquifers (>300 m) are generally considered safe [14]. Thus, there is a rising interest towards detecting the hazardous effects of arsenic on aquatic species and its indirect consequences on human health [15], as well as finding novel innovations to reduce its toxicity.

Conventional physical adsorption, membrane separation or ion exchange, oxidation or coagulation using chemical substances, precipitation, and phytoremediation methods remove As from contaminated water [16], but microbial-based As bioremediation techniques are cutting-edge and cost-effective. Microorganisms are essential in the process of bioremediation because they can break down complex organic compounds into simpler substances [17]. The application of microorganisms in bioremediation is a captivating subject that has been extensively researched by scientists from various fields, such as microbiology, environmental science, and biotechnology [18]. Specific microbial strains have the potential to break down As compounds into less harmful forms and may live in polluted sites because of their metabolic features [11]. Several investigations proved the efficiency of Arsenite oxidation employing Thermus species [19], methylation of arsenite using genetically modified Pseudomonas putida [20] and As adsorption via Escherichia coli [21] as well as converting its toxic form (As III) into low bio-accumulative and toxic chemical forms. It has been previously verified that genetically engineered bacterial strains had greater As bioaccumulation efficiency than natural bacterial strains [22]. Thus, it is vital to investigate genetic factors that have highly successful As adsorption capability and susceptibility in heterologous hosts. Moreover, the use of genetically engineered bacterial strains in bioremediation offers numerous advantages. These include low costs, eco-friendly properties, and a socially acceptable approach for the sustainable elimination of heavy metal waste [23]. However, genetically engineered microbes for bioremediation have not been extensively utilized in the treatment of natural water bodies or aquaculture farms. The main reason for this is that they are generally not permitted to be released into the surrounding waters [[24], [25], [26]]. In particular, the application of microorganisms in bioremediation has various obstacles, such as the high danger of creating secondary chemicals and the discharge of modified genes into natural habitats, which must be resolved before adoption [27]. Subsequently, researchers might ensure the secure application of genetically engineered microbes for As bioremediation using technological protections and suitable approval regulations, such as accomplishing thorough risk assessments and monitoring [28]. Accordingly, bioremediation is a research-critical approach that requires detailed knowledge of microbial modes of action [29].

As mentioned above, numerous studies have thoroughly examined the various forms of arsenic and the role of genetically modified bacterial strains in remedying arsenic contamination in different environments [18,30]. However, there is still a lack of understanding regarding As contamination, discharge into aquatic bodies, bioaccumulation, and bioremediation mechanisms specifically in aquatic systems. With this in mind, the present review aims to achieve two objectives: (1) provide a concise overview of As discharge and contamination in aquatic environments, as well as the application of biotechnology in water treatments, and (2) discuss the potential benefits of utilizing gene encoding techniques to create genetically modified bacterial strains that are highly effective in bioremediation. Furthermore, we will analyze the main challenges that arise when utilizing genetically modified organisms (GMOs) in water treatment, focusing specifically on marine and freshwater environments.

2 Discharge of arsenic into aquatic bodies

Arsenic arises via mother natural mechanisms, including erosion of lava flows, stones containing As and some other biological and human activities, such as operations related to mining, electroplating, metal smelting and application of synthetic fertilizer and/or pesticide in aquatic areas [31]. According to earlier reports, As levels in surface and groundwater near smelting and sulfide mining locations might fluctuate from 100 to 5000 μg/L [32]. Meanwhile, larger quantities of As (1386 up to 5850 μg/L) have been detected offshore near hydrothermal systems [33]. Thus, arsenic pollution of aquatic environments is considered a serious ecological hazard, impacting over 115 countries worldwide [34].

In surface water regions, arsenic is converted into complex chemical compounds. Specifically, there are two main forms of inorganic As types consist of arsenate (As V) and arsenite (As III) [35]. In addition, there are many complicated forms of organic As types such as, dimethylarsinate (DMA), methylarsonate (MA), trimethylarsine oxide (TMAO), tetramethylarsine (TMA), arsenobetaine (AsB), arsenocholine (AsC), arsenosugars (As-Sug), thiolated arsenic, and arsenolipids [36]. After releasing As into water bodies, it has an enormous adverse impact on aquatic species (Table 1), either directly via drinking and breathing or indirectly through increased absorption levels throughout the natural food chain [37]. Additionally, arsenic may threaten consumer health by contaminating drinking water or accumulating into aquatic by-products [38]. Worldwide, from 94 to 220 million individuals, with the vast majority (94 %) living in Asian nations, may be vulnerable to very high amounts of As accumulating in groundwater [39]. According to the US Food and Drug Administration, human consumers may acquire 90 % of the total As by consuming marine fish and other seafood products [40]. Thus, knowing both the biological and ecological pathways of As is very important.Table 1 The adverse effects of arsenic contaminated water bodies on aquatic creatures.

Table 1Arsenic forum	Aquatic species	level	Duration	Biological effect	References	
Arsenic and inorganic arsenic	macroalgae species L. digitata and S. latissima	(41 mg kg−1 and 43 mg kg−1, respectively)	Chronic	Oxidative stress, metabolic disturbances, and histological alterations in the gills and liver.	[41]	
As(V)	Marine juvenile fish Terapon jarbua	50 μg/L	2, 4, 6, and 8 h	The marine fish primarily converted the accumulated As(V) into the non-toxic organic arsenic compound known as arsenobetaine (AsB).	[42]	
Arsenobetaine and arsenate	The marine grouper (E. fuscoguttatus)	500 mL of freshly prepared solutions of AsB (500 μg of AsB added as C5H11AsO2) and As(V) [500 μg of As(V) added as Na2HAsO4·7H2O] were added to 500 g of unmodified food pellets, respectively.	14 days	AsB exhibited a diminished capacity for passing through the intestinal membranes, resulting in sluggish absorption and eventual storage in muscle. In contrast, As(V) demonstrated rapid crossing of the intestinal membranes, swift transportation, and elimination.	[43]	
Inorganic As species (As(III) and As(V))	Marine herbivorous fish Siganus fuscescens	400 and 1500 μg As(III) or As(V) g−1 (dry weight)	21 days and 42 days	It was showed that both inorganic forms of arsenic, As(III) and As(V), present in the diet, were capable of undergoing biotransformation into the less harmful compound arsenobetaine (AsB). This biotransformation occurred to a range of 63.3 %–91.3 % in the liver and 79.0 %–95.2 % in the muscle.	[44]	
Arsenate (As(V)) and arsenite (As(III)	Freshwater fish crucian carp (Carassius auratus)	50 and 100 μg As(III) or As(V) g−1 (dry weight)	10 days and 20 days	The conversion of As(V) to As(III) and the conversion of As(III) to As(V) took place in fish that were fed with As(V) and As(III) respectively.	[45]	

Research has demonstrated that the concentration of different forms of arsenic (As) in freshwater ecological systems is influenced by the process of biodilution [46]. However, in marine habitats, the concentration is more closely related to the enrichment of organic forms, specifically arseno-betaine. Consequently, this leads to the deterioration of food containing high levels of arseno-sugar [47]. Particularly, AsB is regarded as the outcome of As degradation in the marine live food cycle, although mechanistic knowledge of its biodegradation and production remains limited [48]. Several variables influence arsenic bio-absorption by aquatic creatures, including aquatic species, organism weight and age, as well as some ecological aspects such as salinity, pH, phosphorus, and dissolved organic matter (DOM) concentrations [35]. In addition, there are some factors related to the nature of the aquatic organism that affect arsenic transformation into food chain including the rate of ingestion, the gut's entire environment, the gut passage time, aquatic species, the consuming rate of living prey, stocking density, pH value, and iron oxides concentration [49]. Furthermore, various physiological activities including reproduction, excretion, and molting contribute to the body's elimination of As [50]. Besides, the density of live feed, pre-exposures, prey types, and phosphate level might influence the As elimination efficiency [51]. Thus, it is vital to highlight the available knowledge on the bioaccumulation of As to generate a single, unified resource for future research.

3 Mechanisms of bacterial bioremediation for arsenic

Bacteria are very resistant to difficult environmental conditions and might live by maintaining varied biological processes, allowing them to thrive and grow in severe habitats [52]. Multiple bacterial strains have the potential to grow well in arsenic-contaminated environments and exhibit diverse arsenic detoxification pathways via multiple methods that allow them to avoid the harmful effects caused by arsenic [53]. The list of some bacterial stains applied for arsenic remediation is summarized in Table 2 content. Several reports demonstrated several bacterial detoxification processes against arsenic pollution, including the production of exopolysaccharide (EPS), complexation via specific proteins, reduction or oxidation reactions, precipitation, methylation process, metal chelating, cellular surface adsorption or biosorption mechanisms, metal entrapment by cellular capsulation, and active biological transportation [54,55]. These detoxification pathways of arsenic may be applied for bioremediation of arsenic. In order to effectively remove arsenic from aquatic wastewater using gene-transforming bacterial strains, a deep understanding of all the processes involved in this method is essential. Therefore, the following are the arsenic bioremediation methods identified in various bacteria (Fig. 1), allowing microorganisms to be used in wastewater treatment applications.Table 2 The list of bacterial stains applied for arsenic remediation.

Table 2Bacterial strain	Arsenic level (mg/L)	Arsenic form	Bioremediation mechanisms	Remediation rate (%)	Maximum pH value	Incubation maximum Temperature degree	References	
Exiguobacterium profundum	71,924.73 or 600	As5+ or As3+	Biosorption	N/A	7	37	[56]	
Bacillus aryabhatti	37,500	As5+	Reduction	N/A	7	60	[57]	
Micrococcus sp.	44,953	As5+	Oxidation	N/A	9	30	[58]	
Bacillus flexus	11,239 or 5245	As5+ or As3+	Biosorption	8	8	30	[59]	
Acineto bacterjunii	11,239 or 5245	As5+ or As3+	Bioaccumulation	14	8	30	[60]	
Bacillus indicus	22,477 or 150	As5+ or As3+	Bioaccumulation	N/A	7	37	[61]	
Acineto bacterlwoffii	26,223 or 375	As5+ or As3+	Bioaccumulation	N/A	7	30	[62]	
Acinetobacter sp.	29,969 or 375	As5+ or As3+	Bioaccumulation	N/A	9	30	[62]	
Acinetobacter sp.	26,223 or 1124	As5+ or As3+	oxidation	N/A	7	37	[63]	
Exiguobacterium sp.	26,223 or 750	As5+ or As3+	Oxidation and reduction	N/A	7	30	[64]	
Bacillus spp.	74,922 or 5245	As5+ or As3+	Oxidation and reduction	88.74	10	30	[65]	
Pseudomonas sp.	974	As5+	Oxidation	100	7	30	[66]	
Pseudomonas sp.	1124	As3+	reduction	100	7	30	[67]	
Providenciarettgeri	1000	As5+	Bioremediation	N/A	8.5	35	[68]	
Pseudomonas chengduensis	20280 or 3250	As5+ or As3+	reduction	48–78	6	37	[69]	
Acinetobacterl woffii	9365 or 3746	As5+ or As3+	Bioremediation	N/A	7	30	[59]	
Leclerciaadecarboxylata	7492 or 750	As5+ or As3+	reduction	100	7.5	37	[66]	
Pseudomonas aeruginosa	7000 or 1400	As5+ or As3+	Biosorption	98	7	30	[70]	
Bacillus cereus	3000	N/A	Bioaccumulation	83.81	7	30	[71]	
Lysinibacillusbor Onitolerans	3000	N/A	Bioaccumulation	85.72	7.5	30	[72]	
Delftia spp.	74,922 or 5245	As5+ or As3+	oxidation	91.04	7	37	[70]	
Micrococcus sp.	29,969 or 1873	As5+ or As3+	oxidation	39.22	7	30	[73]	

Fig. 1 Summarizes the genetic strategies used by genetically modified bacterial cells to identify biotransformation, reduction, and oxidation pathways in aquatic environments contaminated with arsenic. These strategies include the use of specific genes and operons.

Fig. 1

3.1 Detoxification supported by an active biological transportation activity

The protein transporter generated via the arsP gene can carry the organic form of arsenic directly inside the bacterial cells. Specifically, the arsN1, arsI, and arsH genes generate specific enzymes that participate in organoarsenical detoxification [74]. Few types of bacteria contain arsI gene that is responsible for generating the lyase enzyme, which is capable of breaking down carbon-arsenic bonds and altering organo-arsenicals to Arsenic III [75]. Whereas, the arsH gene could oxidize trivalent aromatic arsenicals and methylated via the organo-arsenical oxidase enzyme and transform them into pentavalent structure form [76].

On the other hand, certain soil bacterial strains convert organo-arsenical to the very poisonous pentavalent form known as arsinothricin [77]. Meanwhile, bacteria developed in arsinothricin-contaminated ecosystems may detoxify arsinothricin compounds by converting α-amino groups to methyl groups through acetylation process [78]. Recent research has shown that E. coli strains include another type of arsN1 gene (PparsN1), which has the potential to convert arsinothricin into a less hazardous form by activation of the acetylation pathways process [79,80].

In addition, bacteria have an operon system, which is a genetic regulatory system that arranges genes encoding similar proteins together with the DNA. This operon system is used by bacteria as a mechanism for bioremediation of heavy metals [81]. In the presence of heavy metals, the regulatory protein associated with the promoter region interacts with the metals, enabling DNA polymerase to bind to the promoter. As a result of this interaction, various systems within the operon, such as efflux systems, conversion systems, and multiple types of resistance systems, are transcribed [82].

Meanwhile, some microbes that are resistant to arsenic can use As V in anaerobic respiration or convert As V to As III as a way to detoxify [83]. The features of these strains of bacteria, which have resistance mechanisms, are encoded by the ars operon. The configuration of the operon varies among different strains [84]. The regulatory protein ArsR, which stimulates the specific binding site for As III; the As V reductase ArsC; and the As III efflux pump ArsB [83]. Whereas, ArsC facilitates the reduction of As V using glutaredoxin, glutathione, or thioredoxin. This detoxification pathway requires ATP as an energy source [85].

In addition, the arr operon consists of two genes, arrA and arrB, which encode the large and small subunits of Arr, respectively. Therefore, Arr is a functional heterodimeric periplasmic protein that requires the expression of both ArrA and ArrB subunits. In bacterial strain ANA-3, Arr expression begins during the exponential growth phase and continues throughout the stationary phase until it is released from the cell [86]. The protein's activity is not activated by electron acceptors such as antimonite, nitrate, selenate, and sulfur [83]. However, recent research has shown that ArrA is specifically induced in the presence of As(V) and acetate in G. lovleyi [87], highlighting the role of these bacteria in releasing arsenic from groundwater sediments.

A recently discovered arx operon, similar to MLHE-1, has been found in the genome of Ectothiorhodospira sp. strain PHS-1 [88]. This bacterium, which is a purple sulfur bacterium, carries out photosynthesis and was isolated from Mono Lake (hydrothermal waters). It can utilize As(III) as an electron donor in anaerobic phototrophy [89]. Another strain, called ML-SRAO and also isolated from Mono Lake, can anaerobically oxidize As (III) and reduce selenite [90]. Unlike MLHE-1, ML-SRAO cannot grow autotrophically, but it can develop heterotrophically on lactate using As V as the electron acceptor. The absence of As III oxidase gene amplification and the positive amplification of the arrA gene from strain ML-SRAO indicate that arrA, like MLHE-1, functions as an oxidoreductase [83].

Finally, resistant bacterial strains have an aio operon in their genome structure, which is responsible for the oxidation pathways of As (III) [91]. In the same context, Hao et al. [92] reported the presence of the aio operon involved in As (III) oxidation within the genome of A. tumefaciens 5A (As (III)-oxidizing strain). The expression of this operon is regulated by a two-component signal transduction system and quorum sensing [92].

3.2 Biosorption pathways

Biosorption is an effective method used for eliminating pollutants from contaminated environments [93]. Microorganisms can biosorb arsenic because of their more advanced cell wall architecture [59]. Because of the abundance of arsenic-binding regions on the bacterial cell wall, arsenic biosorption increased notably throughout the early stages of bacterial growth. The biosorption of arsenic decreased in late bacterial developmental stages owing to increasing the saturation of heavy metal sites of binding [56]. Bacterial fluids produced in reaction to As assist aggregate As from the environment onto its cell membrane [56].

The biosorption of As relies on the binding of As containing a positive charge with the bacterial cell wall or extracellular fluids having a negative charge [94]. Besides, some function groups remain within the bacterial cell wall actively biosorbent Arsenic III, such as carboxyl, hydroxyl, amine, and amide [95]. Furthermore, the bacterial cell wall biofilm may operate to serve as an effective biosorbent agent for the As owing to the presence of a high quantity of exopolysaccharides [56]. For instance, Exiguobacterium profundum demonstrated elevated As biosorption efficiency in both planktonic and biofilm forms [56].

There are several factors have been influencing the bacterial biosorption efficiency of As such as ecological factors (for instance, pH, temperature, etc.), the bacterial biomass chemical structure and solution physicochemical features [93]. It was investigated that Arsenic V biosorption rate significantly reduced with higher ambient temperature [96]. The influence of ambient temperature on biosorption effectiveness might be attributed to the diminishing of physical properties and instability of the surface of the adsorbent at higher degrees [96]. Meanwhile, the solution's pH directly impacts arsenic biosorption by altering the bacterial functional groups and the arsenic form [96]. In alkaline solution, the As biosorption significantly decreased with higher pH values. While, bacterial cell wall exhibits high As ш biosorption in acidic environments between pH 4–7 with increasing the bacterial negative charge to bind As ш positive charge [93]. Thus, controlling environmental variables might enhance the biosorption rate for As remediation.

Several bacterial strains have shown the biosorption efficiency of arsenic. Isolated bacterial stains from groundwater, such as Pseudomonas aeruginosa, demonstrated higher biosorption efficiency (90.72 %) towards arsenic, decreasing it from 10,000 down to 928 ppb in 30 min. Also, increasing incubation time enlarged biosorption efficiency (97.92 %) down to 208 ppb in 2 h [67]. Moreover, E. Profundum is exhibited to have As biosorption capability [56]. In addition, fermented bio-waste by Corynebacterium glutamicum covered with polyethylenimine has shown higher biosorption efficacy, removing 62.99 mg per g of As V [96]. Meanwhile, employing Yersinia sp. dead cells showed higher biosorption efficiency (47 %) of Arsenic III in 80 min under an acidic environment [97].

3.3 Bioaccumulation

Bioaccumulation in bacteria is a metabolic mechanism that requires energy to absorb heavy metals within the cell and accumulate them in its cytoplasm [59]. Bacteria can transfer arsenic from polluted areas into their cells by a variety of methods, including exchange of ions, medium transport, channels of ionization, endocytosis, and fat permeability [[98], [99], [100]]. Besides, Arsenic might be retained within the cellular cytoplasm in a variety of forms, including meta-arsenite, free arsenic, arsenate, and ortho-arsenite [101]. These arsenic types might be connected to entire cellular biomolecules or retained in lipid vacuoles to eliminate their cellular negative effects [102]. Recently, it was explored that deactivating certain enzymes, such as arsenate reductase and modifying the bacterial cell efflux routes (ACR3) enhanced arsenic bioaccumulation within the cell [103]. For instance, the absence of aCR3 and arsenate reductase improved C. glutamicum's arsenic bioaccumulation capability by 28–30 times [98]. Furthermore, the particular protein transporter upregulation (GlpF) enhances arsenic bioremediation, subsequently increasing the bacterial bioaccumulation performance [101]. Moreover, bacterial stains developed in an arsenic-contaminated aquatic solution with 100 ppm of Arsenic V or Arsenic III showed higher bioaccumulation capacity throughout the log phase of development [7]. Whereas, Pseudomonas and Exiguobacterium showed higher arsenic bioaccumulation efficiency up to 17.58 and 19.66 mg per g during 24 h, respectively [104]. Thus, microorganisms having a high potential for arsenic bioaccumulation may be beneficial for arsenic bioremediation in polluted locations.

4 Biotechnology's role in arsenic bioremediation

Numerous biotechnological methodologies characterize the efficacy of identified molecular impact on As remediation [7]. In recent decades, scientists have produced genetically altered microbes that are resistant to and accumulate arsenic. The main microbial genetically modified strains applied in arsenic bioremediation were summarized in Table 3 content. For instance, it had been previously demonstrated that the Bacillus subtilis 168 strains modified genetically using the upregulation of the CmarsM gene (arsenite S-adenosylmethionine methyltransferase) from the alga Cyanidioschyzon merolae resistance to overheating showed a higher ability to volatilize and methylate arsenic [73]. Heterologous upregulation of ArsM from Rhodopseudomonas palustris conferred As III tolerance to an arsenic-sensitive strain of E. coli. While, ArsM catalysis is the synthesis of a variety of methylated intermediates from As III, resulting in trimethylarsine. The end result is the removal of As from both the medium and the cells [105]. It was found that the arsenic M gene was markedly upregulated in Bacillus idriensis and Sphingomonas desiccabilis [106]. Furthermore, it was demonstrated that genetically modified microorganisms with highly upregulated arsenic M gene can accumulate Arsenic (for instance, from 2.2 up to 4.5 % in the soil and more than 10-fold in aquatic solution nutrients) via bio-volatilization compared to the natural bacterial strains [28]. Meanwhile, modified Bacillus subtilis 168 strains through overexpression of the CmarsM gene turned the arsenic into its methylated form (trimethylarsine and dimethylarsenate oxide) or converted it into volatilized form (trimethylarsine and dimethylarsine) [55]. Also, when the genetically engineered bacterial strains were put into arsenic-polluted organic waste for 48 h, they transformed inorganic arsenic into its volatilization form and produced methylated organic molecules [54]. All of the above-mentioned investigations evaluated the successful function of using genetically modified microbes for bioremediation of Arsenic-polluted compost. The genetically engineered Corynebacterium glutamicum stain resistance to arsenic demonstrated optimized bioremediation removal efficiency of arsenic [107]. Specifically, the genetically engineered Corynebacterium glutamicum stain converted arsenic via mycothiol-based single-cysteine reductase into two major forms (Arsenic C1 and Arsenic C2) [72]. Also, the genetically modified Corynebacterium glutamicum strain has the potential to create three-cysteine homodimer Arsenic C1, boosted by the arsenic 1 operon, which has a constitutive function to boost Arsenic (V) absorption in this strain [108]. Thus, the genetically engineered Corynebacterium glutamicum strains were capable to bioremediate 30-fold more arsenic (V) and 15-fold more arsenic (lll) compared to the untreated group [109].Table 3 The main microbial genetically modified strains applied in arsenic bioremediation.

Table 3Strain	Family	Bioaccumulation efficiency	Expressed genes	References	
Desulfovibirio desulfuricans	Desulfovibrionaceae	Biomineralizes pyrite for arsenic removal	Not identified	[110]	
Paraclostridium sp. EML	Clostridiaceae	This bacterium is capable of methylating arsenic under anaerobic circumstances and effectively detoxifying the resulting compound.	arsM	[111]	
Pseudomonas (AK1 and AK9)	Pseudomonadaceae	The presence of aoxR, aoxB, and aoxC genes in both isolated strains AK1 and AK9 has been established. These genes are crucial in the process of arsenic bioremediation through the oxidation of arsenite.	aoxR, aoxB and aoxC	[112]	
Pseudomonas alcaligenes	Pseudomonadaceae	This strain has the capability to methylate and volatilize arsenite.	arsB	[44]	
KG1D and PF14	Pseudomonadaceae	The organism undergoes oxidation of hazardous arsenic, exhibits tolerance towards several other heavy metals, and effectively eliminates arsenic.	arsRBC	[95]	
Rhodococcus sp. TS1, Delftia sp. TS33, Delftia sp. TS41, Streptomyces lividans sp. PSQ22 and Comamonas sp. TS37	Nocardiaceae, Comamonadaceae, and Streptomycetaceae	Arsenate-reducing mechanism	Not identified	[113]	
Brevibacterium linens strain AE038-8	Brevibacteriaceae	Extremely arsenic-resistant and can reduce As V to As III in specific conditions.	aCR3, arsC, arsR and two isolated types of arsO	[114]	
Achromobacter xylosoxidans BHW-15	Alcaligenaceae	This strain has the ability bioaccumulate and detoxify trivalent arsenic.	aioA	[115]	

Meanwhile, it was previously observed that amplification of the arsenic R gene in bacterial strains with elastin-like polypeptide (ELP153AR) boosted arsenic bioaccumulation throughout their cells 60-fold compared to non-modified bacterial cells [116]. Genetically modified E. coli cells with higher upregulation of the arsR gene optimized the effectiveness of its bioremediation removal properties up to 100 % of the arsenite (50 ppb) in the polluted site [104], indicating that genetically modified organisms indicate a less expensive and more efficient technique for future applications in bioremediation of arsenic. In Pseudomonas putida strain KT2440, the overexpression of arsR1 and arsR2, the primary two arsenic-sensitive inhibitors, indicated their function as regulatory triggers in arsenite and arsenate resistance [20]. In vitro analysis of the aforementioned genes showed that one regulator form (arsR1 or arsR2) inhibits the other [117]. The present investigation proposes that the presence of Arsenic R gene mutations in the bacterial cells influences their adaptive role as suppressor genes of arsenic resistance [118].

5 Applying gene encoding techniques to produce genetically modified bacterial strains

Several genetic engineering methods at the gene or genome level have been employed to insert, remove, or substitute one or more nucleotides into bacterial DNA fragments to generate genetically engineered bacterial strains. Recently, CRISPR-Cas (clustered regularly interspaced short palindromic repeats-associated nucleases) techniques have been developed to be an effective and simple gene editing approach [119]. Meanwhile, certain DNA-binding application techniques have been implemented at the entire genome level, such as TALEN (transcription activators like effector nucleases), which is nucleotide sequences particular to the host genome [120]. While, the DSBs (Double-stranded breaks) approaches were developed for stabilizing the DNA fragments produced by the TALEN process [121]. Additionally, the ZFNs (Zinc-finger nucleases) method was used in conjunction with the presence of 30 amino acids to increase DNA bending dominance [122]. Furthermore, the FokI DNA cleavage domain has played a pivotal role in the success of ZFNs and later TALENs [123].

Therefore, two major approaches (TALENs and ZFNs) have arisen in parallel to cope with the molecular complications of nucleases [118]. Consequently, the technique known as CRISPR-Cas is capable of editing multiple genes rapidly with a high precision degree [23]. Recently, several attempts have been made to apply CRISPR-Cas tools in microorganisms like E. coli or Pseudomonas, or even non-model bacterium strains like Comamonas testosteroni and Achromobacter sp. HZ01 to determine its bioremediation effectiveness in arsenic bioremediation via verifying the generation of gRNA that encodes function-altered specific genes relevant to the remediation process [104]. Specifically, CRISPR-Cas9 could be employed to delete or insert the specific gene of interest in the bacterial strain to stimulate its bioremediation efficiency [124]. For example, removing the yvmC gene from Bacillus licheniformis cell via the CRISPR-Cas9 technique, raising its bioremediation efficiency to 100 % [125]. Thus, CRISPR-Cas9 technology could be employed soon to create new strains of microbes capable of bioremediating arsenic in the aquatic environment.

Besides, metabolic engineering techniques could enhance the bioremediation efficiency of bacterial strains by inserting specific genes responsible for up-regulating the synthesis of particular enzymes such as esterases, oxidases, phenoloxidases, monooxygenases, and oxidoreductases that are responsible for a bacterial enzyme-based bioremediation method (called green method) [59]. As mentioned above, the arsenic detoxifying pathway is regulated by ArsC-encoding genes, which stimulate proteins that promote the reduction of Arsenic V into Arsenic III using arsenate reductase enzyme in the cytoplasm [126], followed by Arsenic decontaminate removal from the cytoplasm by an outflow channel [19]. Thus, the availability of metabolic pathway information is vital in determining the microbial bioremediation efficiency of heavy metals.

6 The awareness regarding the wide application of genetically altered bacteria in arsenic bioremediation

There are many issues and restrictions with using genetically modified bacteria for arsenic bioremediation that hinder its widespread use in ecological areas. Major drawbacks or restrictions with bioremediation applications using engineered bacterial strains include (1) the possibility of creating secondary metabolites and leakage of genetically modified genes into aquatic systems, which must still be disclosed before widespread commercial use. Researchers compared the maximum documented levels of accumulation of arsenic in the published literature and discovered that wild live bacteria could accumulate 9.80 ± 0.50 mg As/g dry-weight bacteria [71], but engineered strains could accumulate 7.59 mg As/g dry-weight bacteria [127]. Therefore, it is essential to determine the genetic factors that have a high sensitivity and ability to stimulate arsenic adsorption in heterogeneous hosts [111]. Also, (2) it is important to carefully analyze the different distribution of contaminants in treated areas since this might lead to an unbalanced scattering of the gas or liquid generated by applied modified bacteria. Because acceptable levels of decontamination are being achieved at different sites at a slower rate, it is difficult to predict with certainty how biological remediation will be employed widely in open areas with expected success [28]. Furthermore, (3) the release of genetically engineered bacterial stains into open areas is a complex procedure that has to adhere to strict guidelines and get authorization from several ethical and regulatory organizations [95]. Thus, utilizing genetically engineered bacterial strains for bioremediation is a cutting-edge technique that involves extensive knowledge of the metabolic pathways of the microbial population.

7 Conclusion and future directions

Arsenic (As) is a heavy metal metallic ion found in aquatic systems as a consequence of both natural (volcanic eruptions, fires in forests, and rock erosion) and human activities (including the wastes of paint, medication, herbicide, shampoo, and electronics industries). It is a substantial and widespread environmental pollutant that has direct and indirect health consequences on all living creatures. Thus, complete or partial elimination of this heavy metal from water bodies is a critical process for ecological remediation in many regions. There are various technologies suggested for removing arsenic from aquatic environments, including precipitation using chemicals, exchange of ions, adsorption, filtration through membranes, botanical remediation, bacterial bioremediation, and electrocoagulation. Several recent reports have proven that the efficacy of employing bacterial strains for arsenic bioremediation of contaminated water improved significantly after modifying the genetic structure of these bacteria. Specifically, genetically engineered bacterial strains can boost the quantity of released enzymes that can break down both inorganic and organic forms of arsenic in the aquatic environment. Until now, additional investigations were required to identify the specific bacterial strains that have a high ability to break down inorganic arsenic contaminants.

The water quality criteria (such as, pH and ambient temperature fluctuation) are the major issue that should be thoroughly examined to maintain high bacterial bioremediation efficiency. In addition, further studies are required to determine the ideal ambient temperature and other water physical requirements for the breakdown of arsenic molecules in natural water bodies. Furthermore, understanding the relationship between the water ambient temperature degree and the incubation temperature necessary for bacterial growth to survive in the aquatic environment is critical. This could help prevent the failure of arsenic bioremediation when releasing or mobilizing exogenous modified bacterial strains into an aquatic environment.

Thus, it is necessary to undertake more research to prove the safety of employing genetically modified organisms in wastewater treatment by evaluating all environmental implications that may occur via mutation and other processes. Therefore, regulatory agencies should be established to monitor any potential problems associated with genetically altered bacterial species, especially in aquatic environments, as well as encourage lawmakers and public people to support this bioremediation technique.

Ethical approval

Not applicable for review studies.

Funding

Not applicable.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Data availability statement

The collected literature applied and/or presented during the current study is available from the corresponding author (Mohammed A.E. Naiel) on reasonable request.

CRediT authorship contribution statement

Mohammed A.E. Naiel: Writing – review & editing, Writing – original draft, Formal analysis, Data curation, Conceptualization. Ehab S. Taher: Funding acquisition, Formal analysis. Fatema Rashed: Investigation, Funding acquisition. Shakira Ghazanfar: Funding acquisition, Formal analysis. Abdelrazeq M. Shehata: Validation, Software. Nourelhuda A. Mohammed: Validation, Supervision. Raul Pascalau: Methodology, Formal analysis. Laura Smuleac: Visualization, Validation. Ateya Megahed Ibrahim: Software, Resources, Project administration. Ahmed Abdeen: Writing – original draft, Supervision, Software, Investigation. Mustafa Shukry: Visualization, Resources, Methodology.

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.

Acknowledgement

This literature was supported via 10.13039/100009392 Prince Sattam bin Abdulaziz University project number (PSAU/2024 /R/1445), Al-Kharj, Saudi Arabia. Also, this literature is funded partially by 10.13039/501100010272 Zarqa University -Jordan and 10.13039/100022866 Mutah University , Jordan. This paper is published from the own research funds of the University of Life Sciences “King Mihai I” from Timisoara, Romania.
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References

1 Mehana E.-S.E. Khafaga A.F. Elblehi S.S. Abd El-Hack M.E. Naiel M.A. Bin-Jumah M. Othman S.I. Allam A.A. Biomonitoring of heavy metal pollution using acanthocephalans parasite in ecosystem: an updated overview Animals 10 2020 811 10.3390/ani10050811 32392878
2 Gharib A.A. Abdel-Hamid E.A. Mousa M.A. Naiel M.A. Improving water quality, growth performance, and modulating some stress physiological biomarkers in Cyprinus carpio using raw date nuclei as a zinc adsorbent agent Appl. Water Sci. 12 2022 159 10.1007/s13201-022-01682-8
3 Naiel M.A. Negm S.S. Ghazanfar S. Farid A. Shukry M. Acrylamide toxicity in aquatic animals and its mitigation approaches: an updated overview Environ. Sci. Pollut. Res. 30 2023 113297 113312
4 Naiel M.A. Shehata A.M. Negm S.S. Abd El‐Hack M.E. Amer M.S. Khafaga A.F. Bin‐Jumah M. Allam A.A. The new aspects of using some safe feed additives on alleviated imidacloprid toxicity in farmed fish: a review Rev. Aquacult. 12 2020 225.2267- 0
5 Abd El-hameed S.A Negm S.S. Ismael N.E. Naiel M.A. Soliman M.M. Shukry M. Abdel-Latif H.M. Effects of activated charcoal on growth, immunity, oxidative stress markers, and physiological responses of Nile tilapia exposed to sub-lethal imidacloprid toxicity Animals 11 2021 1357 10.3390/ani11051357 34064658
6 Xue Y. Li Y. Li X. Zheng J. Hua D. Jiang C. Yu B. Arsenic bioremediation in mining wastewater by controllable genetically modified bacteria with biochar Environ. Technol. Innov. 33 2024 103514
7 Preetha J.S.Y. Arun M. Vidya N. Kowsalya K. Halka J. Ondrasek G. Biotechnology advances in bioremediation of arsenic: a review Molecules 28 2023 1474 36771138
8 Plewniak F. Crognale S. Rossetti S. Bertin P.N. A genomic outlook on bioremediation: the case of arsenic removal Front. Microbiol. 9 2018 358244
9 Bertin P.N. Crognale S. Plewniak F. Battaglia-Brunet F. Rossetti S. Mench M. Water and soil contaminated by arsenic: the use of microorganisms and plants in bioremediation Environ. Sci. Pollut. Control Ser. 29 2021 9462 9489
10 Brewster M.D. Removing arsenic from contaminated wastewater Water Environ. Technol. 4 1992 54 57
11 Khan A. Asif I. Abid R. Ghazanfar S. Ajmal W. Shehata A. Naiel M. The sustainable approach of microbial bioremediation of arsenic: an updated overview Int. J. Environ. Sci. Technol. 21 2024 7849 7864
12 Dilpazeer F. Munir M. Baloch M.Y.J. Shafiq I. Iqbal J. Saeed M. Abbas M.M. Shafique S. Aziz K.H.H. Mustafa A. A comprehensive review of the latest advancements in controlling arsenic contaminants in groundwater Water 15 2023 478
13 Shaji E. Santosh M. Sarath K. Prakash P. Deepchand V. Divya B. Arsenic contamination of groundwater: a global synopsis with focus on the Indian Peninsula Geosci. Front. 12 2021 101079
14 Huq M.E. Fahad S. Shao Z. Sarven M.S. Khan I.A. Alam M. Saeed M. Ullah H. Adnan M. Saud S. Arsenic in a groundwater environment in Bangladesh: occurrence and mobilization J. Environ. Manag. 262 2020 110318
15 Tolkou A.K. Toubanaki D.K. Kyzas G.Z. Detection of arsenic, chromium, cadmium, lead, and mercury in fish: effects on the sustainable and healthy development of aquatic life and human consumers Sustainability 15 2023 16242
16 Irshad S. Xie Z. Mehmood S. Nawaz A. Ditta A. Mahmood Q. Insights into conventional and recent technologies for arsenic bioremediation: a systematic review Environ. Sci. Pollut. Control Ser. 28 2021 18870 18892
17 Laha A. Sengupta S. Bhattacharya P. Mandal J. Bhattacharyya S. Bhattacharyya K. Recent advances in the bioremediation of arsenic-contaminated soils: a mini review World J. Microbiol. Biotechnol. 38 2022 189 35972701
18 Hui C.-y. Liu M.-q. Guo Y. Synthetic bacteria designed using ars operons: a promising solution for arsenic biosensing and bioremediation World J. Microbiol. Biotechnol. 40 2024 192 38709285
19 Gihring T.M. Druschel G.K. McCleskey R.B. Hamers R.J. Banfield J.F. Rapid arsenite oxidation by Thermus aquaticus and Thermus thermophilus: field and laboratory investigations Environ. Sci. Technol. 35 2001 3857 3862 11642444
20 Chen J. Qin J. Zhu Y.-G. de Lorenzo V.c. Rosen B.P. Engineering the soil bacterium Pseudomonas putida for arsenic methylation Appl. Environ. Microbiol. 79 2013 4493 4495 23645194
21 Ke C. Zhao C. Rensing C. Yang S. Zhang Y. Characterization of recombinant E. coli expressing arsR from Rhodopseudomonas palustris CGA009 that displays highly selective arsenic adsorption Appl. Microbiol. Biotechnol. 102 2018 6247 6255 29789881
22 Rafeeq H. Afsheen N. Rafique S. Arshad A. Intisar M. Hussain A. Bilal M. Iqbal H.M. Genetically engineered microorganisms for environmental remediation Chemosphere 310 2023 136751
23 Chen S.-C. Sun G.-X. Yan Y. Konstantinidis K.T. Zhang S.-Y. Deng Y. Li X.-M. Cui H.-L. Musat F. Popp D. The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling Proc. Natl. Acad. Sci. USA 117 2020 10414 10421 32350143
24 Liu S. Zhang F. Chen J. Sun G. Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions J. Environ. Sci. 1550 –1544 2011 23
25 Bartley D.M. Hallerman E.M. A global perspective on the utilization of genetically modified organisms in aquaculture and fisheries Aquaculture 137 1995 1 7
26 Hallerman E.M. Kapuscinski A.R. Incorporating risk assessment and risk management into public policies on genetically modified finfish and shellfish Aquaculture 137 1995 9 17
27 Sher S. Rehman A. Use of heavy metals resistant bacteria—a strategy for arsenic bioremediation Appl. Microbiol. Biotechnol. 103 2019 6007 6021 31209527
28 Kabiraj A. Biswas R. Halder U. Bandopadhyay R. Bacterial arsenic metabolism and its role in arsenic bioremediation Curr. Microbiol. 79 2022 131 35290506
29 Sizova O.I. Kochetkov V.V. Validov S.Z. Boronin A.M. Kosterin P.V. Lyubun Y.V. Arsenic-contaminated soils genetically modified Pseudomonas spp. and their arsemc-phytoremediation potential J. Soils Sediments 2 2002 19 23
30 Lee S.Y. Kim Y. Kang S.A. Chang B. Hur H. Lee Y.J. Characterization of arsenic (III and V) adsorption on natural schwertmannite formed in acid coal mine drainage: batch studies and spectroscopic observations J. Environ. Chem. Eng. 11 2023 109170
31 Williams P.N. Lei M. Sun G. Huang Q. Lu Y. Deacon C. Meharg A.A. Zhu Y.-G. Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: hunan, China Environ. Sci. Technol. 43 2009 637 642 19244995
32 Rahman M.A. Hasegawa H. Lim R.P. Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain Environ. Res. 116 2012 118 135 22534144
33 Breuer C. Pichler T. Arsenic in marine hydrothermal fluids Chem. Geol. 348 2013 2 14
34 Medunić G. Fiket Ž. Ivanić M. Arsenic contamination status in Europe, Australia, and other parts of the world Arsenic in Drinking Water and Food 2020 183 233
35 Byeon E. Kang H.-M. Yoon C. Lee J.-S. Toxicity mechanisms of arsenic compounds in aquatic organisms Aquat. Toxicol. 237 2021 105901
36 Xiong X. Zhang K. Chen Y. Qu C. Wu C. Arsenic in water, sediment, and fish of lakes from the Central Tibetan Plateau J. Geochem. Explor. 210 2020 106454
37 Raman R.K. Talukder A. Mahanty A. Sarkar D.J. Das B.K. Bhowmick S. Samanta S. Manna S.K. Mohanty B.P. Arsenic bioaccumulation and identification of low-arsenic-accumulating food fishes for aquaculture in arsenic-contaminated ponds and associated aquatic ecosystems Biol. Trace Elem. Res. 200 2022 2923 2936 34467440
38 Naiel M.A.-E. Shehata A.M. Paswan V.K. Said M.B. El-Tarabily K.A. Utilizing the potential of Saussurea lappa in aquaculture industry: a review on immune enhancement and pollution remediation Aquacult. Int. 2024 1 38 10.1007/s10499-024-01435-1
39 Mukherjee A. Sengupta M.K. Hossain M.A. Ahamed S. Das B. Nayak B. Lodh D. Rahman M.M. Chakraborti D. Arsenic contamination in groundwater: a global perspective with emphasis on the Asian scenario J. Health Popul. Nutr. 2006 142 163 17195556
40 Mullard A. 2017 FDA drug approvals Nat. Rev. Drug Discov. 17 2018 81 86 29348678
41 Maulvault A.L. Anacleto P. Barbosa V. Sloth J.J. Rasmussen R.R. Tediosi A. Fernandez-Tejedor M. van den Heuvel F.H. Kotterman M. Marques A. Toxic elements and speciation in seafood samples from different contaminated sites in Europe Environ. Res. 143 2015 72 81 26411778
42 Zhang W. Huang L. Wang W.-X. Arsenic bioaccumulation in a marine juvenile fish Terapon jarbua Aquat. Toxicol. 105 2011 582 588 21945928
43 Xiong H. Tan Q.-G. Zhang J. Wang W.-X. Yuan X. Zhang W. Yan B. Physiologically based pharmacokinetic model revealed the distinct bio-transportation and turnover of arsenobetaine and arsenate in marine fish Aquat. Toxicol. 240 2021 105991
44 Zhang W. Chen L. Zhou Y. Wu Y. Zhang L. Biotransformation of inorganic arsenic in a marine herbivorous fish Siganus fuscescens after dietborne exposure Chemosphere 147 2016 297 304 26766368
45 Cui D. Zhang P. Li H. Zhang Z. Luo W. Yang Z. Biotransformation of dietary inorganic arsenic in a freshwater fish Carassius auratus and the unique association between arsenic dimethylation and oxidative damage J. Hazard Mater. 391 2020 122153
46 Ghosh D. Ghosh A. Bhadury P. Arsenic through aquatic trophic levels: effects, transformations and biomagnification—a concise review Geoscience Letters 9 2022 20
47 Caumette G. Koch I. Reimer K. Arsenobetaine formation in plankton: a review of studies at the base of the aquatic food chain J. Environ. Monit. 14 2012 2841 2853 23014956
48 Agbabiaka L. Diyaolu D. Obisike E. Accumulation and human health risk analysis of arsenic, lead, and mercury in three fishes caught from an oil-polluted-creek in Niger Delta, Nigeria Iran. J. Fish. Sci. 23 2024 223 235
49 Magellan K. Barral-Fraga L. Rovira M. Srean P. Urrea G. García-Berthou E. Guasch H. Behavioural and physical effects of arsenic exposure in fish are aggravated by aquatic algae Aquat. Toxicol. 156 2014 116 124 25190483
50 Tuulaikhuu B.-A. Bonet B. Guasch H. Effects of low arsenic concentration exposure on freshwater fish in the presence of fluvial biofilms Sci. Total Environ. 544 2016 467 475 26657392
51 Datta S. Ghosh D. Saha D.R. Bhattacharaya S. Mazumder S. Chronic exposure to low concentration of arsenic is immunotoxic to fish: role of head kidney macrophages as biomarkers of arsenic toxicity to Clarias batrachus Aquat. Toxicol. 92 2009 86 94 19237206
52 Naiel M.A. Abdelghany M.F. Khames D.K. Abd El-hameed S.A. Mansour E.M. El-Nadi A.S. Shoukry A.A. Administration of some probiotic strains in the rearing water enhances the water quality, performance, body chemical analysis, antioxidant and immune responses of Nile tilapia, Oreochromis niloticus Appl. Water Sci. 12 2022 209 10.1007/s13201-022-01733-0
53 Akmal U. Ghori I. Elasbali A.M. Alharbi B. Farid A. Alamri A.S. Muzammal M. Asdaq S.M.B. Naiel M.A. Ghazanfar S. Probiotic and antioxidant potential of the Lactobacillus spp. isolated from artisanal fermented pickles Fermentation 8 2022 328
54 Akhtar M.S. Chali B. Azam T. Bioremediation of arsenic and lead by plants and microbes from contaminated soil Research in Plant Sciences 1 2013 68 73
55 Bahar M.M. Megharaj M. Naidu R. Bioremediation of arsenic-contaminated water: recent advances and future prospects Water, Air, Soil Pollut. 224 2013 1 20
56 Saba R. Andreasen Li Y. Rehman Y. Ahmed M. Meyer R. Sabri A. Prospective role of indigenous Exiguobacterium profundum PT2 in arsenic biotransformation and biosorption by planktonic cultures and biofilms J. Appl. Microbiol. 124 2018 431 443 29130635
57 Khanam R. Moni R. Islam M. Billah M. Zohora U. Sabrin F. Rahman M. Study of an arsenic metabolizing bacteria from arsenic contaminated soil of Chandpur district, Bangladesh Jahangirnagar University Journal of Biological Sciences 8 2019 57 65
58 Bhakat K. Chakraborty A. Islam E. Characterization of arsenic oxidation and uranium bioremediation potential of arsenic resistant bacteria isolated from uranium ore Environ. Sci. Pollut. Res. 26 2019 12907 12919
59 Marwa N. Singh N. Srivastava S. Saxena G. Pandey V. Singh N. Characterizing the hypertolerance potential of two indigenous bacterial strains (Bacillus flexus and Acinetobacter junii) and their efficacy in arsenic bioremediation J. Appl. Microbiol. 126 2019 1117 1127 30556924
60 Rahman M.S. Jamal M.A.H.M. Biswas P.K. Rahman S.M. Sharma S.P. Saha S.K. Hong S.T. Islam M.R. Arsenic remediation in Bangladeshi rice varieties with enhance plant growth by unique arsenic-resistant bacterial isolates Geomicrobiol. J. 37 2020 130 142
61 Zannier F. Portero L.R. Ordoñez O.F. Martinez L.J. Farías M.E. Albarracin V.H. Polyextremophilic bacteria from high altitude Andean lakes: arsenic resistance profiles and biofilm production BioMed Res. Int. 2019 2019
62 Biswas R. Sarkar A. Characterization of arsenite-oxidizing bacteria to decipher their role in arsenic bioremediation Prep. Biochem. Biotechnol. 49 2019 30 37 29889593
63 Kale S. Salaskar D. Ghosh S. Sounderajan S. Isolation and identification of arsenic resistant Providencia rettgeri (KDM3) from industrial effluent contaminated soil and studies on its arsenic resistance mechanisma J. Microb. Biochem. Technol. 7 2015 194 201
64 Jebelli M.A. Maleki A. Amoozegar M.A. Kalantar E. Shahmoradi B. Gharibi F. Isolation and identification of indigenous prokaryotic bacteria from arsenic-contaminated water resources and their impact on arsenic transformation Ecotoxicol. Environ. Saf. 140 2017 170 176 28259061
65 Banerjee S. Datta S. Chattyopadhyay D. Sarkar P. Arsenic accumulating and transforming bacteria isolated from contaminated soil for potential use in bioremediation Journal of Environmental Science and Health, Part A 46 2011 1736 1747
66 Han Y.-H. Yin D.-X. Jia M.-R. Wang S.-S. Chen Y. Rathinasabapathi B. Chen D.-L. Ma L.Q. Arsenic-resistance mechanisms in bacterium Leclercia adecarboxylata strain As3-1: biochemical and genomic analyses Sci. Total Environ. 690 2019 1178 1189 31470481
67 Tariq A. Ullah U. Asif M. Sadiq I. Biosorption of arsenic through bacteria isolated from Pakistan Int. Microbiol. 22 2019 59 68 30810933
68 Aguilar N.C. Faria M.C. Pedron T. Batista B.L. Mesquita J.P. Bomfeti C.A. Rodrigues J.L. Isolation and characterization of bacteria from a brazilian gold mining area with a capacity of arsenic bioaccumulation Chemosphere 240 2020 124871
69 Biswas R. Majhi A.K. Sarkar A. The role of arsenate reducing bacteria for their prospective application in arsenic contaminated groundwater aquifer system Biocatal. Agric. Biotechnol. 20 2019 101218
70 Tanmoy P. Chakraborty A. Islam E. Mukherjee S.K. Arsenic bioremediation potential of arsenite-oxidizing Micrococcus sp. KUMAs15 isolated from contaminated soil Pedosphere 28 2018 299 310
71 Joshi D.N. Flora S. Kalia K. Bacillus sp. strain DJ-1, potent arsenic hypertolerant bacterium isolated from the industrial effluent of India J. Hazard Mater. 166 2009 1500 1505 19233553
72 Ghosh S. Sarkar B. Genetically modified bacteria for arsenic bioremediation Genomics Approach to Bioremediation: Principles, Tools, and Emerging Technologies 2023 467 483 10.1002/9781119852131.ch25
73 Dey U. Chatterjee S. Mondal N.K. Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation Biotechnology reports 10 2016 1 7 28352518
74 Ben Fekih I. Zhang C. Li Y.P. Zhao Y. Alwathnani H.A. Saquib Q. Rensing C. Cervantes C. Distribution of arsenic resistance genes in prokaryotes Front. Microbiol. 9 2018 2473 30405552
75 Nadar V.S. Yoshinaga M. Pawitwar S.S. Kandavelu P. Sankaran B. Rosen B.P. Structure of the ArsI C–As Lyase: insights into the mechanism of degradation of organoarsenical herbicides and growth promoters J. Mol. Biol. 428 2016 2462 2473 27107642
76 Yang H.-C. Rosen B.P. New mechanisms of bacterial arsenic resistance Biomed. J. 39 2016 5 13 27105594
77 Kuramata M. Sakakibara F. Kataoka R. Yamazaki K. Baba K. Ishizaka M. Hiradate S. Kamo T. Ishikawa S. Arsinothricin, a novel organoarsenic species produced by a rice rhizosphere bacterium Environ. Chem. 13 2016 723 731
78 Kuramata M. Sakakibara F. Kataoka R. Abe T. Asano M. Baba K. Takagi K. Ishikawa S. Arsenic biotransformation by S treptomyces sp. isolated from rice rhizosphere Environ. Microbiol. 17 2015 1897 1909 25039305
79 Nadar V.S. Chen J. Dheeman D.S. Galván A.E. Yoshinaga-Sakurai K. Kandavelu P. Sankaran B. Kuramata M. Ishikawa S. Rosen B.P. Arsinothricin, an arsenic-containing non-proteinogenic amino acid analog of glutamate, is a broad-spectrum antibiotic Commun. Biol. 2 2019 131 30993215
80 Li Y.P. Ben Fekih I. Chi Fru E. Moraleda-Munoz A. Li X. Rosen B.P. Yoshinaga M. Rensing C. Antimicrobial activity of metals and metalloids Annu. Rev. Microbiol. 75 2021 175 197 34343021
81 Saravanan A. Kumar P.S. Ramesh B. Srinivasan S. Removal of toxic heavy metals using genetically engineered microbes: molecular tools, risk assessment and management strategies Chemosphere 298 2022 134341
82 Somayaji A. Sarkar S. Balasubramaniam S. Raval R. Synthetic biology techniques to tackle heavy metal pollution and poisoning Synthetic and Systems Biotechnology 7 2022 841 846 35572766
83 Cavalca L. Corsini A. Zaccheo P. Andreoni V. Muyzer G. Microbial transformations of arsenic: perspectives for biological removal of arsenic from water Future Microbiol. 8 2013 753 768 23586329
84 Páez-Espino D. Tamames J. de Lorenzo V. Cánovas D. Microbial responses to environmental arsenic Biometals 22 2009 117 130 19130261
85 Ordonez E.n. Letek M. Valbuena N. Gil J.A. Mateos L.M. Analysis of genes involved in arsenic resistance in Corynebacterium glutamicum ATCC 13032 Appl. Environ. Microbiol. 71 2005 6206 6215 16204540
86 Keren R. Méheust R. Santini J.M. Thomas A. West-Roberts J. Banfield J.F. Alvarez-Cohen L. Global genomic analysis of microbial biotransformation of arsenic highlights the importance of arsenic methylation in environmental and human microbiomes Comput. Struct. Biotechnol. J. 20 2022 559 572 36284711
87 Giloteaux L. Holmes D.E. Williams K.H. Wrighton K.C. Wilkins M.J. Montgomery A.P. Smith J.A. Orellana R. Thompson C.A. Roper T.J. Characterization and transcription of arsenic respiration and resistance genes during in situ uranium bioremediation The ISME journal 7 2013 370 383 23038171
88 Zargar K. Conrad A. Bernick D.L. Lowe T.M. Stolc V. Hoeft S. Oremland R.S. Stolz J. Saltikov C.W. ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductases Environ. Microbiol. 14 2012 1635 1645 22404962
89 Kulp T. Hoeft S. Asao M. Madigan M. Hollibaugh J. Fisher J. Stolz J. Culbertson C. Miller L. Oremland R. Arsenic (III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California Science 321 2008 967 970 18703741
90 Fisher J.C. Hollibaugh J.T. Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California Appl. Environ. Microbiol. 74 2008 2588 2594 18326681
91 Cai L. Liu G. Rensing C. Wang G. Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils BMC Microbiol. 9 2009 1 11 19121223
92 Hao X. Lin Y. Johnstone L. Liu G. Wang G. Wei G. McDermott T. Rensing C. Genome sequence of the arsenite-oxidizing strain Agrobacterium tumefaciens 5A Am Soc Microbiol. 194 2012 10.1128/jb.06585-11
93 Haris S.A. Altowayti W.A.H. Ibrahim Z. Shahir S. Arsenic biosorption using pretreated biomass of psychrotolerant Yersinia sp. strain SOM-12D3 isolated from Svalbard, Arctic Environ. Sci. Pollut. Res. Int. 25 2018 27959 27970 30062542
94 Altowayti W.A.H. Salem A.A. Al-Fakih A.M. Bafaqeer A. Shahir S. Tajarudin H.A. Optimization of as (V) removal by dried bacterial biomass: nonlinear and linear regression analysis for isotherm and kinetic modelling Metals 12 2022 1664
95 Roy V. Saha B.K. Adhikary S. Chaki M.G. Sarkar M. Pal A. Isolation, characterization, identification, genomics and analyses of bioaccumulation and biosorption potential of two arsenic-resistant bacteria obtained from natural environments Sci. Rep. 14 2024 5716 38459150
96 Kim N. Park M. Yun Y.-S. Park D. Removal of anionic arsenate by a PEI-coated bacterial biosorbent prepared from fermentation biowaste Chemosphere 226 2019 67 74 30913429
97 Altowayti W.A.H. Algaifi H.A. Bakar S.A. Shahir S. The adsorptive removal of as (III) using biomass of arsenic resistant Bacillus thuringiensis strain WS3: characteristics and modelling studies Ecotoxicol. Environ. Saf. 172 2019 176 185 30708229
98 Pandey N. Keshavkant S. Characterization of arsenic resistant plant‐growth promoting indigenous soil bacteria isolated from Center‐East regions of India J. Basic Microbiol. 59 2019 807 819 31070248
99 Briffa J. Sinagra E. Blundell R. Heavy metal pollution in the environment and their toxicological effects on humans Heliyon 6 2020 e04691 10.1016/j.heliyon.2020.e04691
100 Bhat S.A. Hassan T. Majid S. Heavy metal toxicity and their harmful effects on living organisms–a review International Journal of Medical Science And Diagnosis Research 3 2019 106 122
101 Satyapal G.K. Rani S. Kumar M. Kumar N. Potential role of arsenic resistant bacteria in bioremediation: current status and future prospects J. Microb. Biochem. Technol. 256–258 2016 8
102 Sevak M.P. Pushkar B. Bacterial responses towards arsenic toxicity and in-depth analysis of molecular mechanism along with possible on-field application J. Environ. Chem. Eng. 11 2023 110187
103 Sevak P. Pushkar B. Arsenic pollution cycle, toxicity and sustainable remediation technologies: a comprehensive review and bibliometric analysis J. Environ. Manag. 349 2024 119504
104 Saltikov C.W. Olson B.H. Homology of Escherichia coli R773 arsA, arsB, and arsC genes in arsenic-resistant bacteria isolated from raw sewage and arsenic-enriched creek waters Appl. Environ. Microbiol. 68 2002 280 288 11772637
105 Qin J. Rosen B.P. Zhang Y. Wang G. Franke S. Rensing C. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase Proc. Natl. Acad. Sci. USA 103 2006 2075 2080 16452170
106 González-Benítez N. Durante-Rodríguez G. Kumar M. Carmona M. Biotechnology for arsenic detection and bioremediation Front. Microbiol. 12 2021 743109
107 Maleki F. Shahpiri A. Efficient and specific bioaccumulation of arsenic in the transgenic Escherichia coli expressing ArsR1 from Corynebacterium glutamicum Biometals 5 2022 889 901
108 Liu Y. Zeng Y. Yang J. Chen P. Sun Y. Wang M. Ma Y. A bioflocculant from Corynebacterium glutamicum and its application in acid mine wastewater treatment Front. Bioeng. Biotechnol. 11 2023 1136473
109 Li X. Liu Y. Zhong J. Che C. Gong Z. Si M. Yang G. Molecular mechanisms of Mycoredoxin-1 in resistance to oxidative stress in Corynebacterium glutamicum J. Gen. Appl. Microbiol. 67 2021 15 23 33148889
110 Duverger A. Berg J.S. Busigny V. Guyot F. Bernard S. Miot J. Mechanisms of pyrite formation promoted by sulfate-reducing bacteria in pure culture Front. Earth Sci. 8 2020 588310
111 Viacava K. Qiao J. Janowczyk A. Poudel S. Jacquemin N. Meibom K.L. Shrestha H.K. Reid M.C. Hettich R.L. Bernier-Latmani R. Meta-omics-aided isolation of an elusive anaerobic arsenic-methylating soil bacterium The ISME journal 16 2022 1740 1749 35338334
112 Satyapal G.K. Mishra S.K. Srivastava A. Ranjan R.K. Prakash K. Haque R. Kumar N. Possible bioremediation of arsenic toxicity by isolating indigenous bacteria from the middle Gangetic plain of Bihar, India Biotechnology reports 17 2018 117 125 29541605
113 Yang Q. Tu S. Wang G. Liao X. Yan X. Effectiveness of applying arsenate reducing bacteria to enhance arsenic removal from polluted soils by Pteris vittata L Int. J. Phytoremediation 14 2012 89 99 22567697
114 Maizel D. Blum J.S. Ferrero M.A. Utturkar S.M. Brown S.D. Rosen B.P. Oremland R.S. Characterization of the extremely arsenic-resistant Brevibacterium linens strain AE038-8 isolated from contaminated groundwater in Tucumán, Argentina Int. Biodeterior. Biodegrad. 107 2016 147 153
115 Diba F. Khan M.Z.H. Uddin S.Z. Istiaq A. Shuvo M.S.R. Ul Alam A.R. Hossain M.A. Sultana M. Bioaccumulation and detoxification of trivalent arsenic by Achromobacter xylosoxidans BHW-15 and electrochemical detection of its transformation efficiency Sci. Rep. 11 2021 21312
116 Zhou X. Kang F. Qu X. Fu H. Alvarez P.J. Tao S. Zhu D. Role of extracellular polymeric substances in microbial reduction of arsenate to arsenite by Escherichia coli and Bacillus subtilis Environ. Sci. Technol. 54 2020 6185 6193 32315521
117 Páez‐Espino A.D. Nikel P.I. Chavarría M. de Lorenzo V. ArsH protects Pseudomonas putida from oxidative damage caused by exposure to arsenic Environ. Microbiol. 22 2020 2230 2242 32202357
118 Chen J. Sun G.-X. Wang X.-X. Lorenzo V.c.d. Rosen B.P. Zhu Y.-G. Volatilization of arsenic from polluted soil by Pseudomonas putida engineered for expression of the arsM arsenic (III) S-adenosine methyltransferase gene Environ. Sci. Technol. 48 2014 10337 10344 25122054
119 Liu W. Li L. Jiang J. Wu M. Lin P. Applications and challenges of CRISPR-Cas gene-editing to disease treatment in clinics Precision clinical medicine 4 2021 179 191 34541453
120 Sun N. Zhao H. Transcription activator‐like effector nucleases (TALENs): a highly efficient and versatile tool for genome editing Biotechnol. Bioeng. 110 2013 1811 1821 23508559
121 Shamshirgaran Y. Liu J. Sumer H. Verma P.J. Taheri-Ghahfarokhi A. Tools for efficient genome editing; ZFN, TALEN, and CRISPR Applications of genome modulation and editing 2495 2022 2946 10.1007/978-1-0716-2301-5_2
122 Qi Y. Zhang Y. Zhang F. Baller J.A. Cleland S.C. Ryu Y. Starker C.G. Voytas D.F. Increasing frequencies of site-specific mutagenesis and gene targeting in Arabidopsis by manipulating DNA repair pathways Genome Res. 23554–547 2013
123 Chandrasegaran S. Carroll D. Origins of programmable nucleases for genome engineering J. Mol. Biol. 428 2016 963 989 26506267
124 Mu Y. Zhang C. Li T. Jin F.-J. Sung Y.-J. Oh H.-M. Lee H.-G. Jin L. Development and applications of CRISPR/Cas9-based genome editing in Lactobacillus Int. J. Mol. Sci. 23 2022 12852
125 Zhan Y. Xu Y. Zheng P. He M. Sun S. Wang D. Cai D. Ma X. Chen S. Establishment and application of multiplexed CRISPR interference system in Bacillus licheniformis Appl. Microbiol. Biotechnol. 104 2020 391 403 31745574
126 Mukhopadhyay R. Rosen B.P. Arsenate reductases in prokaryotes and eukaryotes Environ. Health Perspect. 745–748 2002 110
127 Ma Y. Lin J. Zhang C. Ren Y. Lin J. Cd (II) and as (III) bioaccumulation by recombinant Escherichia coli expressing oligomeric human metallothioneins J. Hazard Mater. 185 2011 1605 1608 21074318
