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Bacterial metabolism of environmental arsenic - Mechanisms and biotechnological applications
Abstract and Figures
Arsenic causes threats for environmental and human health in numerous places around the world mainly due to its carcinogenic potential at low doses. Removing arsenic from contaminated sites is hampered by the occurrence of several oxidation states with different physicochemical properties. The actual state of arsenic strongly depends on its environment whereby microorganisms play important roles in its geochemical cycle. Due to its toxicity, nearly all organisms possess metabolic mechanisms to resist its hazardous effects, mainly by active extrusion, but also by extracellular precipitation, chelation, and intracellular sequestration. Some microbes are even able to actively use various arsenic compounds in their metabolism, either as an electron donor or as a terminal electron acceptor for anaerobic respiration. Some microorganisms can also methylate inorganic arsenic, probably as a resistance mechanism, or demethylate organic arsenicals. Bioavailability of arsenic in water and sediments is strongly influenced by such microbial activities. Therefore, understanding microbial reactions to arsenic is of importance for the development of technologies for improved bioremediation of arsenic-contaminated waters and environments. This review gives an overview of the current knowledge on bacterial interactions with arsenic and on biotechnologies for its detoxification and removal.
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... The uptake of As(III) and As(V) by microorganisms are generally described through aquaglyceroporin and phosphate transporters (Pi), respectively, since the chemical structure of As(III) and As(V) resemble the substrates of these transporters (Kruger et al. 2013;Garbinski et al. 2019). In bacteria, there are two phosphate transporters involved for As(V), Pit, and Pst (Tsai et al. 2009;Jia et al. 2019). ...
... An example is Escherichia coli, where arsenic is taken up through the nonspecific phosphate transporter Pit. Other bacteria may express a specific phosphate transporter, Pst, which is less efficient in arsenate transport (Kruger et al. 2013). On the other hand, As(III) is taken up by a member of the glycerol channels of the major intrinsic protein (MIP) family, called the glycerol transporter GlpF (Yan et al. 2019). ...
... On the other hand, As(III) is taken up by a member of the glycerol channels of the major intrinsic protein (MIP) family, called the glycerol transporter GlpF (Yan et al. 2019). In addition, the transport of As(V) is considered as an active transport in contrast with As(III) where no energy is necessary to pass through the membrane (Kruger et al. 2013). Fungi and yeast possess homology mechanisms of As uptake from those identified in bacterial cells. ...
... In aquatic ecosystems, arsenic usually exists in the form of inorganic species of arsenate, As (V), and arsenite, As (III). Eh-potential and pH of the environment are the most important factors influencing the state and transformation of the above arsenic forms [5,[156][157][158][159][160][161]. Under anaerobic (reducing) conditions and at low Eh-potential, As (III) dominates, while under aerobic (oxidative) conditions, As(V) dominates. ...
... Under anaerobic (reducing) conditions and at low Eh-potential, As (III) dominates, while under aerobic (oxidative) conditions, As(V) dominates. In oxygen-free sulphide systems, when Eh-potential decreases to −250 mV, thioarsenites and thioarsenates may predominate, accounting for about 83% of the total arsenic content [160,161]. The arsenate species, in turn, are determined by the pH of the aquatic environment. ...
... At pH <6.9, H 2 AsO -4 predominates, while at higher pH values, HAsO 2-4 does [5,156]. Arsenic is one of the few chemical elements having mutagenic and carcinogenic effects on living organisms [5,156,157,[159][160][161]. However, its toxicity, like many others elements, depends on the species in the aquatic environment [4,156]. ...
... The ars operon contains an organised set of genes necessary for arsenic resistance. The ars operon consists of arsRBC and arsRDABC genes (Kruger et al. 2013). The arsRBC gene system encodes the arsB, an integral protein, acting as a membrane arsenite permease pump, arsR, encodes for regulatory repressor protein and arsC, encodes for arsenate reductase, involved in the detoxification of As by reducing arsenate to arsenite. ...
Unlabelled:
Enterobacter cloacae RSC3 isolated from an industrial pesticide site transformed arsenate into arsenite. The arsenate is transported by membrane-bound phosphate transporter and transformed to arsenite by arsenate reductase (arsC). E. cloacae RSC3 produced an arsenate reductase enzyme with a maximum activity of 354 U after 72 h of incubation. Arsenate reductase was found to be active and stable at a wide range of temperatures (20 and 45 °C) and pH (5-10), with maximum activity at 35 °C and pH 7.0. The arsenate reductase protein was further characterised molecularly using different bioinformatics tools. The 3D structure of ArsC protein was predicted by homology modelling and validated by the Ramachandran plot with 91.9% residues in the most favoured region. ArsC protein of E. cloacae RSC3 revealed structural homology with ArsC from PDB ID: 1S3C. The gene ontology results also showed that the ArsC protein had a molecular functionality of the arsenate reductase (glutaredoxin) activity and the biological function of cellular response to DNA damage stimulus. Molecular docking analysis of 3D structures using AutoDock vina-1.5.7 server predicted four ligand binding active site residues at Gln70, Asp68, Leu68, and Leu63. Strong ArsC-arsenate ion interaction was observed with binding energy -1.03 kcal/mol, indicating significant arsenate reductase activity and specificity of ArsC protein. On the basis of molecular dynamics simulation analysis, the RMSD and RMSF values revealed the stability of ArsC protein from E. cloacae RSC3.
Supplementary information:
The online version contains supplementary material available at 10.1007/s13205-023-03730-9.
... The respiratory oxidization of As(III) to As(V) and the reduction of As(V) to As(III) are represented by the aio/arx (light pink) and arr systems (dark pink), respectively. Uptake of As(V) and As(III) is represented by phosphate transporters (Pit or Pst) and by aquaglycerolporins (GlpF) (brown) (Adapted from [183]). The figure was partly generated using Servier Medical Art, provided by Servier, licensed under a Creative Commons Attribution 3.0 unported license. ...
Antimicrobial resistance (AMR) has a significant global impact on human, animal, and environmental health. Misuse and overuse of antibiotics in clinical and animal production settings are the main drivers behind the emergence of antimicrobial resistant bacteria. However, other compounds with antimicrobial activity may also contribute to this global public health problem. The aim of this comprehensive review is to provide detailed insights into the impact of metals and organic acids on the emergence and spread of AMR in the food chain, for which their role is not fully understood. The review examines the widespread use of organic acids in the food industry as feed additives or disinfectants, the crucial role of copper in animal growth and the harmful effects of mercury and arsenic as pollutants in food-producing environments. Additionally, it explores the antimicrobial mechanisms of metals and organic acids, the tolerance mechanisms developed by bacteria, and the interplay between genes responsible for metal tolerance and AMR. The comprehensive and integrated data presented highlights the need to further explore and understand the role of metals and organic acids as drivers of AMR to develop well-defined strategies effectively mitigating the AMR crisis within the food chain context.
... pyrite), exacerbating the mobilization and dispersion of arsenic (Shaji et al., 2021;Smith et al., 2019;Zhi et al., 2021). The elevated arsenic concentrations may affect microbial reductive dehalogenation via various pathways: shortcircuiting oxidative phosphorylation, inhibiting enzymatic activities by binding to thiol groups, or directly inducing the disassembly of Fe\ \S clusters in proteins (Kruger et al., 2013). Gushgari-Doyle and Alvarez-Cohen (2020) indicated that As(V) and As(III) have differential inhibitory impacts on TCE dechlorination of Dehalococcoides mccartyi (Gushgari-Doyle and Alvarez-Cohen, 2020). ...
Inorganic arsenic and organochlorines are frequently co-occurring contaminants in anoxic groundwater environments, and the bioremediation of their composite pollution has long been a rigorous predicament. Currently, the dechlorination behaviors and stress responses of microbial dechlorination consortia to arsenic are not yet fully understood. This study assessed the reductive dechlorination performance of a Dehalococcoides-bearing microcosm DH under gradient concentrations of arsenate [As(V)] or arsenite [As(III)] and investigated the response patterns of different functional microorganisms. Our results demonstrated that although the dechlorination rates declined with increasing arsenic concentrations in both As(III/V) scenarios, the inhibitory impact was more pronounced in As(III)-amended groups compared to As(V)-amended groups. Moreover, the vinyl chloride (VC)-to-ethene step was more susceptible to arsenic exposure compared to the trichloroethene (TCE)-to-dichloroethane (DCE) step, while high levels of arsenic exposure [e.g. As(III) > 75 μM] can induce significant accumulation of VC. Functional gene variations and microbial community analyses revealed that As(III/V) affected reductive dechlorination by directly inhibiting organohalide-respiring bacteria (OHRB) and indirectly inhibiting synergistic populations such as acetogens. Metagenomic results indicated that arsenic metabolic and efflux mechanisms were identical among different Dhc strains, and variations in arsenic uptake pathways were possibly responsible for their differential responses to arsenic exposures. By comparison, fermentative bacteria showed high potential for arsenic resistance due to their inherent advantages in arsenic detoxification and efflux mechanisms. Collectively, our findings expanded the understanding of the response patterns of different functional populations to arsenic stress in the dechlorinating consortium and provided insights into modifying bioremediation strategies at co-contaminated sites for furtherance.
... Due to the mimicking properties of TTE, they can unwantedly enter the plant body via several nutrient uptake mechanisms. For example, As(V) has the properties of PO 4 3− (Kruger et al., 2013), because As(V) enters into the cell through phosphate transport, whereas As(III) enters through the glycerol transport system (Rosen, 2002). Similarly, Cr mimics the properties of SO 4 2− and PO 4 3− , and cellular uptake occurs via transporters of sulfate and phosphate (O'Brien et al., 2003). ...
Due to various anthropogenic activities, soil pollution with TTE and consequent degradation of soil quality are increasing. The harmful effects of TTE eventually affect humans via consumption of edible plants grown on such contaminated sites. In the search for economically and environmentally viable techniques for TTE remediation, biological approaches that combine endophytic
microbes and plants have shown promising outcomes in recent years. Endophytic microbes assist the plant partner in mitigating the effect of TTE and other biotic and abiotic stresses by transforming the redox state of elements; inducing defense molecules, enzymes, and hormones; and regulating the uptake of ionic elements by plants. Identification of suitable organisms and conditions for enhancing the TTE remediation potential will bring success to microbe-assisted phytoremediation. Hence, future studies should be carried out to find efficient organisms with high plant colonization efficiency and TTE detoxification potential for applying this promising remediation method under field conditions.
Antimicrobial resistance (AMR) has a significant impact on human, animal, and environmental health, being spread in diverse settings. Antibiotic misuse and overuse in the food chain are widely recognized as primary drivers of antibiotic-resistant bacteria. However, other antimicrobials, such as metals and organic acids, commonly present in agri-food environments (e.g., in feed, biocides, or as long-term pollutants), may also contribute to this global public health problem, although this remains a debatable topic owing to limited data. This review aims to provide insights into the current role of metals (i.e., copper, arsenic, and mercury) and organic acids in the emergence and spread of AMR in the food chain. Based on a thorough literature review, this study adopts a unique integrative approach, analyzing in detail the known antimicrobial mechanisms of metals and organic acids, as well as the molecular adaptive tolerance strategies developed by diverse bacteria to overcome their action. Additionally, the interplay between the tolerance to metals or organic acids and AMR is explored, with particular focus on co-selection events. Through a comprehensive analysis, this review highlights potential silent drivers of AMR within the food chain and the need for further research at molecular and epidemiological levels across different food contexts worldwide.
Since Mn, Fe and As contaminants often coexist in the environment, we hypothesize that the presence of multifunctional bacteria is capable of reducing Mn and Fe oxides and promoting the mobilization and release of arsenic. However, such bacteria have not been reported yet; moreover, the impact of bacteria with the ability to simultaneously reduce Mn and Fe oxides on the formation of high-arsenic groundwater remains unclear. This study aims to address this question. Here, we found that the microbial community in the soils was able to efficiently reduce Mn oxides into Mn(II). An analysis of the microbial community structures of the soil shows that it contained Proteobacteria (41.1%), Acidobacteria (10.9%), Actinobacteria (9.5%) and other less abundant bacteria. Based on this observation, we successfully isolated a novel bacterium Cellulomonas sp. CM1, which possesses both Mn- and Fe-oxide-reducing activities. Under anaerobic conditions, strain CM1 can reduce Mn oxides, resulting in the production of 13 mg/L of Mn(II) within a span of 10 days. Simultaneously, it can reduce Fe oxides, leading to the generation of 9 mg/L of Fe(II) within 9 days when a yeast extract is used as an electron donor. During these reduction reactions, the cells were grown into a density of OD600 0.16 and 0.09, respectively, suggesting that Mn(IV) is more beneficial for the bacterial growth than Fe(III). Arsenic release assays indicate that after 108 days of anoxic incubation, approximately 126.2, 103.2 and 81.5 μg/L As(V) were mobilized and released from three soil samples, respectively, suggesting that CM1 plays significant roles in driving mobilization of arsenic from soils. These findings shed new light on the microbial processes that lead to the generation of arsenic-contaminated groundwater.
Phylogenetic analysis indicates that microbial arsenic metabolism is ancient and probably extends back to the primordial Earth. In microbial biofilms growing on the rock surfaces of anoxic brine pools fed by hot springs containing arsenite and sulfide at high concentrations, we discovered light-dependent oxidation of arsenite [As(III)] to arsenate [As(V)] occurring under anoxic conditions. The communities were composed primarily of Ectothiorhodospira-like purple bacteria or Oscillatoria-like cyanobacteria. A pure culture of a photosynthetic bacterium grew as a photoautotroph when As(III) was used as the sole photosynthetic electron donor. The strain contained genes encoding a putative As(V) reductase but no detectable homologs of the As(III) oxidase genes of aerobic chemolithotrophs, suggesting a reverse functionality for the reductase. Production of As(V) by anoxygenic photosynthesis probably opened niches for primordial Earth's first As(V)-respiring prokaryotes.
Passive treatment systems have a long history in the remediation of mining impacted water. The functioning of these systems is poorly understood, in particular the microbial processes that underpin metal removal. A biologically based engineered wetland treatment system that has operated in Trail, B.C. to treat seepage from a historic Pb and Zn smelter landfill, was investigated. The system has functioned for more than a decade, an unusually long life span for a passive bioreactor design. The study focuses on the 5a of operation from 2003 until 2007. Arsenic is a major contaminant in the ore that is processed in Trail, which has caused high As concentrations in the seepage. In addition to As, Zn and Cd removal were investigated. During the 5-a period, the system sequestered 2990kg of As, 7700kg of Zn and 85kg of Cd. Nearly 90% of these elements were removed in two biochemical reactors (BCRs) that comprise the first two components of the six cell system, with the remainder removed in plant-based polishing cells. Average input concentrations over the 5-a period were 2.3 and 4.1mM for As and Zn, respectively and 0.45μM for Cd. Final output concentrations were reduced to 0.01mM for As, 0.05mM for Zn and 0.18μM for Cd. Sulfur removal averaged 34% of input concentration. Analysis of mineral formation in the system using X-ray diffraction and scanning electron microscopy indicated kottigite (Zn3(AsO4)2⋅8H2O) and sphalerite (ZnS) as the major mineral phases controlling As and Zn sequestration; Cd appears to be immobilized as CdS. Evidence for orpiment was obtained from X-ray absorption spectroscopy (XANES) studies, and arsenopyrite was not detected. Although microbial activity dominates the removal of Zn, As and Cd from the soluble phase, abiotic removal mechanisms contribute including sorption of As and Zn to biosolids and filtration of metal precipitates by the solid matrix. The removal of toxic elements over the period appeared to be relatively consistent. Seasonal fluctuations, a large spike in input element concentrations over a 2-month period, and removal of the two biochemical reactors during a period of reconstruction appeared to have relatively little impact on the system as a whole.
Microbial biotransformations have a major impact on contamination by toxic elements, which threatens public health in developing and industrial countries. Finding a means of preserving natural environments—including ground and surface waters—from arsenic constitutes a major challenge facing modern society. Although this metalloid is ubiquitous on Earth, thus far no bacterium thriving in arsenic-contaminated environments has been fully characterized. In-depth exploration of the genome of the β-proteobacterium Herminiimonas arsenicoxydans with regard to physiology, genetics, and proteomics, revealed that it possesses heretofore unsuspected mechanisms for coping with arsenic. Aside from multiple biochemical processes such as arsenic oxidation, reduction, and efflux, H. arsenicoxydans also exhibits positive chemotaxis and motility towards arsenic and metalloid scavenging by exopolysaccharides. These observations demonstrate the existence of a novel strategy to efficiently colonize arsenic-rich environments, which extends beyond oxidoreduction reactions. Such a microbial mechanism of detoxification, which is possibly exploitable for bioremediation applications of contaminated sites, may have played a crucial role in the occupation of ancient ecological niches on earth.
Oxyanions of arsenic and selenium call be used in microbial anaerobic respiration as terminal electron accepters. The detection of arsenate and selenate respiring bacteria in numerous pristine and contaminated environments and their rapid appearance in enrichment culture suggest that they are widespread and metabolically active in nature. Although the bacterial species that have been isolated and characterized are still few in number, they are scattered throughout the bacterial domain and include Gram-positive bacteria, beta, gamma and epsilon Proteobacteria and the sole member of a deeply branching lineage of the bacteria, Chrysiogenes arsenatus. The oxidation of a number of organic substrates (i.e. acetate, lactate, pyruvate, glycerol, ethanol) or hydrogen can be coupled to the reduction of arsenate and selenate, but the actual donor used Varies from species to species. Both periplasmic and membrane-associated arsenate and selenate reductases have been characterized. Although the number of subunits and molecular masses differs, they all contain molybdenum. The extent of the environmental impact on the transformation and mobilization of arsenic and selenium by microbial dissimilatory processes is only now being fully appreciated.
Operons coding for the enzyme arsenite oxidase have been detected in the genomes from Archaea and Bacteria by Blast searches using the amino acid sequences of the respective enzyme characterized in two different beta-proteobacteria as templates. Sequence analyses show that in all these species, arsenite oxidase is transported over the cytoplasmic membrane via the tat system and most probably remains membrane attached by an N-terminal transmembrane helix of the Rieske subunit. The biochemical and biophysical data obtained for arsenite oxidase in the green filamentous bacterium Chloroflexus aurantiacus allow a structural model of the enzyme's membrane association to be proposed. Phylogenies for the two constituent subunits (i.e., the molybdopterin-containing and the Rieske subunit) of the heterodimeric enzyme and their respective homologs in DMSO-reductase, formate dehydrogenase, nitrate reductase, and the Rieske/cytb complexes were calculated from multiple sequence alignments. The obtained phylogenetic trees indicate an early origin of arsenite oxidase before the divergence of Archaea and Bacteria. Evolutionary implications of these phylogenies are discussed.
The removal of metals and metalloids occurring in acid mine drainage has been studied on different scales (years, days). Dissolved and particulate concentrations of Fe and As were monitored over a 4-a period along Reigous Creek, an acid mine drainage from a former Pb–Zn mine in southern France. Dissolved concentrations of Fe (12–25mmolL−1), As (0.9–3.5mmolL−1) and SO42- (10–70mmolL−1) exhibited seasonal variations related to rainfall, with an increase during the driest months. About 30% of the As initially present in solution as As(III) was coprecipitated with Fe oxides in the first 40m of Reigous Creek. The corresponding As removal rate was 3.58×10−7molL−1s−1. The mineralogy of resultant precipitates varied spatially and seasonally. Over the first 40m, amorphous As(V)–Fe(III) phases and tooeleite, were formed. Sediments deposited in the bed of the creek close to the spring contained both types of solid phases. Laminated concretions, which consist of precipitates around bacterial structures, were mainly constituted of tooeleite. Further downstream, these Fe-oxide phases were replaced by schwertmannite and ferrihydrite. On a daily basis, concentrations of dissolved Fe and As have been shown to vary up to 10% during the day as a result of photoreduction of Fe-oxide phases.