Genetic identification of arsenate reductase and arsenite oxidase in redox transformations carried out by arsenic metabolising prokaryotes – A comprehensive review

Kumari, Nisha; Jagadevan, Sheeja

doi:10.1016/j.chemosphere.2016.08.044

Cited by 58 publications

(27 citation statements)

References 130 publications

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“…To counter the deleterious effects of these oxyanions, organisms evolved detoxifying, energy-consuming systems [1]. However, certain prokaryotes are also able to use As III (arsenite) and As V (arsenate) as electron donors and acceptors, respectively, for their energy conserving respiratory systems (for reviews, see [2][3][4]).…”

Section: Introductionmentioning

confidence: 99%

The controversy on the ancestral arsenite oxidizing enzyme; deducing evolutionary histories with phylogeny and thermodynamics

Szyttenholm

Chaspoul

Bauzan

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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The three presently known enzymes responsible for arsenic-using bioenergetic processes are arsenite oxidase (Aio), arsenate reductase (Arr) and alternative arsenite oxidase (Arx), all of which are molybdoenzymes from the vast group referred to as the Mo/W-bisPGD enzyme superfamily. Since arsenite is present in substantial amounts in hydrothermal environments, frequently considered as vestiges of primordial biochemistry, arsenite-based bioenergetics has long been predicted to be ancient. Conflicting scenarios, however, have been put forward proposing either Arr/Arx or Aio as operating in the ancestral metabolism. Phylogenetic data argue in favor of Aio whereas biochemical and physiological data led several authors to propose Arx/Arr as the most ancient anaerobic arsenite metabolizing enzymes. Here we combine phylogenetic approaches with physiological and biochemical experiments to demonstrate that the Arx/Arr enzymes could not have been functional in the Archaean geological eon. We propose that Arr reacts with menaquinones to reduce arsenate whereas Arx reacts with ubiquinone to oxidize arsenite, in line with thermodynamic considerations. The distribution of the quinone biosynthesis pathways, however, clearly indicates that the ubiquinone pathway is recent. An updated phylogeny of Arx furthermore reinforces the hypothesis of a recent emergence of this enzyme. We therefore conclude that anaerobic arsenite redox conversion in the Archaean must have been performed in a metabolism involving Aio.

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Section: Introductionmentioning

confidence: 99%

The controversy on the ancestral arsenite oxidizing enzyme; deducing evolutionary histories with phylogeny and thermodynamics

Szyttenholm

Chaspoul

Bauzan

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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“…Moreover, many microorganisms are able to perform a dissimilatory As(V) reduction using As(V) as electron acceptor and different inorganic (e.g., H 2 ) and organic compounds (e.g., small organic acids, sugars and complex aromatic substrates like benzoate and toluene) as electron donor ( Stolz and Oremland, 1999 ; Kumari and Jagadevan, 2016 ). This periplasmic anaerobic respiration of As(V) is driven by a membranous arsenate reductase encoded by arr genes ( Huang, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic Structure and Metabolic Properties of Microbial Communities in Arsenic-Rich Waters of Geothermal Origin

et al. 2017

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Arsenic (As) is a toxic element released in aquatic environments by geogenic processes or anthropic activities. To counteract its toxicity, several microorganisms have developed mechanisms to tolerate and utilize it for respiratory metabolism. However, still little is known about identity and physiological properties of microorganisms exposed to natural high levels of As and the role they play in As transformation and mobilization processes. This work aims to explore the phylogenetic composition and functional properties of aquatic microbial communities in As-rich freshwater environments of geothermal origin and to elucidate the key microbial functional groups that directly or indirectly may influence As-transformations across a natural range of geogenic arsenic contamination. Distinct bacterial communities in terms of composition and metabolisms were found. Members of Proteobacteria, affiliated to Alpha- and Betaproteobacteria were mainly retrieved in groundwaters and surface waters, whereas Gammaproteobacteria were the main component in thermal waters. Most of the OTUs from thermal waters were only distantly related to 16S rRNA gene sequences of known taxa, indicating the occurrence of bacterial biodiversity so far unexplored. Nitrate and sulfate reduction and heterotrophic As(III)-oxidization were found as main metabolic traits of the microbial cultivable fraction in such environments. No growth of autotrophic As(III)-oxidizers, autotrophic and heterotrophic As(V)-reducers, Fe-reducers and oxidizers, Mn-reducers and sulfide oxidizers was observed. The ars genes, involved in As(V) detoxifying reduction, were found in all samples whereas aioA [As(III) oxidase] and arrA genes [As(V) respiratory reductase] were not found. Overall, we found that As detoxification processes prevailed over As metabolic processes, concomitantly with the intriguing occurrence of novel thermophiles able to tolerate high levels of As.

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“…Furthermore, the capacity to reduce As(V) to As(III) as the first stage in a detoxification process has been suggested for some microalgae [53,54,60]. Redox transformations between both inorganic forms of As are quite usual in prokaryotes [86]. However, they have not been well documented in microalgae, although in the C. reinhardtii genome, two arsenate reductase genes were identified, cloned, and expressed on an Escherichia coli strain [87].…”

Section: Analysis Of Mechanisms Involved In Tolerancementioning

confidence: 99%

Toxicity, Physiological, and Ultrastructural Effects of Arsenic and Cadmium on the Extremophilic Microalga Chlamydomonas acidophila

Díaz

Francisco

Olsson³

et al. 2020

IJERPH

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The cytotoxicity of cadmium (Cd), arsenate (As(V)), and arsenite (As(III)) on a strain of Chlamydomonas acidophila, isolated from the Rio Tinto, an acidic environment containing high metal(l)oid concentrations, was analyzed. We used a broad array of methods to produce complementary information: cell viability and reactive oxygen species (ROS) generation measures, ultrastructural observations, transmission electron microscopy energy dispersive x-ray microanalysis (TEM-XEDS), and gene expression. This acidophilic microorganism was affected differently by the tested metal/metalloid: It showed high resistance to arsenic while Cd was the most toxic heavy metal, showing an LC 50 = 1.94 µM. Arsenite was almost four-fold more toxic (LC 50 = 10.91 mM) than arsenate (LC 50 = 41.63 mM). Assessment of ROS generation indicated that both arsenic oxidation states generate superoxide anions. Ultrastructural analysis of exposed cells revealed that stigma, chloroplast, nucleus, and mitochondria were the main toxicity targets. Intense vacuolization and accumulation of energy reserves (starch deposits and lipid droplets) were observed after treatments. Electron-dense intracellular nanoparticle-like formation appeared in two cellular locations: inside cytoplasmic vacuoles and entrapped into the capsule, around each cell. The chemical nature (Cd or As) of these intracellular deposits was confirmed by TEM-XEDS. Additionally, they also contained an unexpected high content in phosphorous, which might support an essential role of poly-phosphates in metal resistance. development of phytoplankton [5][6][7]. However, most of these studies are related to circumneutral pH water environments polluted by industrial and domestic wastes, in spite of the fact that pH has a considerable effect on the availability and, as a consequence, the toxicity of heavy metals [8].Indeed, many freshwater bodies worldwide are highly acidic (pH < 3), either due to natural causes or anthropogenic activities such as mining [9,10]. Acid drainages are due mainly to pyrite oxidation, producing significant acidity in lakes and ponds situated in areas impacted by mining, as well as in rivers receiving mine water discharge [11,12]. Additionally, extreme acidic environments tend to contain unusually high concentrations of heavy metals because their solubility increases markedly as the pH decreases [11]. Despite these extreme environmental conditions, a number of prokaryotic and eukaryotic organisms living in these extreme environments have been identified [13]. Microalgae are the dominant eukaryotes found in these ecosystems, green microalgae such as Chlamydomonas, Dunaliella, and Chlorella being the main primary producers [13].Although acidophilic algae are able to grow at high heavy metal concentrations and low pH, both of which are lethal to most eukaryotes [14], the adaptive mechanisms by which these microorganisms can survive under such environmental conditions are still poorly understood. Proteomic analysis has pointed out the importance of metal and acidity toleranc...

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Genetic identification of arsenate reductase and arsenite oxidase in redox transformations carried out by arsenic metabolising prokaryotes – A comprehensive review

Cited by 58 publications

References 130 publications

The controversy on the ancestral arsenite oxidizing enzyme; deducing evolutionary histories with phylogeny and thermodynamics

The controversy on the ancestral arsenite oxidizing enzyme; deducing evolutionary histories with phylogeny and thermodynamics

Phylogenetic Structure and Metabolic Properties of Microbial Communities in Arsenic-Rich Waters of Geothermal Origin

Toxicity, Physiological, and Ultrastructural Effects of Arsenic and Cadmium on the Extremophilic Microalga Chlamydomonas acidophila

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