Respiratory arsenate reductase as a bidirectional enzyme

Richey, Christine; Chovanec, Peter; Hoeft, Shelley E.; Oremland, Ronald S.; Basu, Partha; Stolz, John F.

doi:10.1016/j.bbrc.2009.03.045

Cited by 102 publications

(81 citation statements)

References 30 publications

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“…The aerobic arsenite oxidases involved in such processes are heterodimers consisting of a large subunit with a molybdenum center and a [3Fe-4S] cluster (AroA, AsoA, and AoxB) and a small subunit containing a Rieske-type [2Fe-2S] cluster (AroB, AsoB, and AoxA) (1, 13). The large subunit in these enzymes is similar to that found in other members of the dimethyl sulfoxide (DMSO) reductase family of molybdenum enzymes but is clearly phylogenetically divergent from the respiratory arsenate reductases (ArrA) or other proteins of the DMSO reductase family of molybdenum oxidoreductases, such as the new arsenite reductase described recently for Alkalilimnicola ehrlichii (25,31,40).aox genes have been identified in 25 bacterial and archaeal genera isolated from various arsenic-rich environments, most of which belong to the Alpha-, Beta-, or Gammaproteobacteria phylum (7,10,12,14,23,25,29,32,37). Recent studies based on environmental DNA extracted from soils, sediments, and geothermal mats with different chemical characteristics and various levels of arsenic contamination have suggested that the distribution and the diversity of arsenite-oxidizing microorganisms may be greater than previously suggested (6, 10, 14-16, 18, 28, 29).…”

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confidence: 55%

Unsuspected Diversity of Arsenite-Oxidizing Bacteria as Revealed by Widespread Distribution of theaoxBGene in Prokaryotes

Heinrich-Salmeron

Cordi

Brochier-Armanet

et al. 2011

Appl Environ Microbiol

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In this study, new strains were isolated from an environment with elevated arsenic levels, Sainte-Marieaux-Mines (France), and the diversity of aoxB genes encoding the arsenite oxidase large subunit was investigated. The distribution of bacterial aoxB genes is wider than what was previously thought. AoxB subfamilies characterized by specific signatures were identified. An exhaustive analysis of AoxB sequences from this study and from public databases shows that horizontal gene transfer has likely played a role in the spreading of aoxB in prokaryotic communities.Arsenic, which is one of the most toxic metalloids, is distributed ubiquitously but not uniformly around the world. Levels of arsenic differ considerably from one geographical region to another, depending on the geochemical characteristics of the soil (natural contamination) and the industrial activities carried out in the vicinity (anthropogenic contamination) (22). In aquatic environments, arsenic occurs mainly in the form of the inorganic species arsenate [As(V)] and arsenite [As(III)]; the latter species, which is more bioavailable, is usually thought to have more-toxic effects on prokaryotes than As(V) (34). As(III) oxidation leads to the formation of the less available form As(V), which can either precipitate with iron [Fe(III)] or be adsorbed by ferrihydrite. The oxidation process may be mediated by microbial activities, which contribute to the natural remediation processes observed in contaminated environments (21,26,27,34). Consequently, bioprocesses for the treatment of arsenic-contaminated waters have been developed based on the precipitation or adsorption of the As(V) produced by bacteria (4, 9, 21). Some well-known prokaryotes oxidize As(III) into As(V) under aerobic (e.g., Herminiimonas arsenicoxydans, Thiomonas spp., or Rhizobium sp. strain NT26) or anaerobic (e.g., Alkalilimnicola ehrlichii) conditions as part of a detoxification process (12,17,31,32,39). Some chemolithotrophs also use arsenite as an electron donor (e.g., Rhizobium sp. strain NT26 or Thiomonas arsenivorans) (5, 32). The aerobic arsenite oxidases involved in such processes are heterodimers consisting of a large subunit with a molybdenum center and a [3Fe-4S] cluster (AroA, AsoA, and AoxB) and a small subunit containing a Rieske-type [2Fe-2S] cluster (AroB, AsoB, and AoxA) (1, 13). The large subunit in these enzymes is similar to that found in other members of the dimethyl sulfoxide (DMSO) reductase family of molybdenum enzymes but is clearly phylogenetically divergent from the respiratory arsenate reductases (ArrA) or other proteins of the DMSO reductase family of molybdenum oxidoreductases, such as the new arsenite reductase described recently for Alkalilimnicola ehrlichii (25,31,40).aox genes have been identified in 25 bacterial and archaeal genera isolated from various arsenic-rich environments, most of which belong to the Alpha-, Beta-, or Gammaproteobacteria phylum (7,10,12,14,23,25,29,32,37). Recent studies based on environmental DNA extracted from soils, sediments, a...

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confidence: 55%

Unsuspected Diversity of Arsenite-Oxidizing Bacteria as Revealed by Widespread Distribution of theaoxBGene in Prokaryotes

Heinrich-Salmeron

Cordi

Brochier-Armanet

et al. 2011

Appl Environ Microbiol

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“…7). Richey et al (20) referred to Mlg_0216 as ArrA for a variety of reasons, such as greater sequence similarity to ArrA than AoxB groups, common biochemical features of ArrA, and the operon structure of mlg_0216 with greater resemblance to arr than aox operons. Despite these observations, we refer to mlg_0216 as arxA because it likely functions as an arsenite oxidase in vivo.…”

Section: Discussionmentioning

confidence: 99%

“…In the arsenite-oxidizing nitrate reducer Alkalilimnicola ehrlichii strain MLHE-1 (a haloalkaliphile isolated from Mono Lake [CA]) (10,15), bioinformatic analysis of its genome revealed the absence of genes homologous to the arsenite oxidase genes of the aoxB type. Instead, two genes (mlg_0216 and mlg_2426) were identified that better resembled the catalytic subunit of the arsenate respiratory reductase (20); however, MLHE-1 has not been shown to respire (or reduce) arsenate (15). Recent work by Richey et al (20) showed that the Mlg_0216 protein (and not Mlg_2426) was expressed under chemolithoautotrophic (10 mM arsenite and 10 mM nitrate) growth conditions.…”

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confidence: 99%

“…Instead, two genes (mlg_0216 and mlg_2426) were identified that better resembled the catalytic subunit of the arsenate respiratory reductase (20); however, MLHE-1 has not been shown to respire (or reduce) arsenate (15). Recent work by Richey et al (20) showed that the Mlg_0216 protein (and not Mlg_2426) was expressed under chemolithoautotrophic (10 mM arsenite and 10 mM nitrate) growth conditions. Moreover, it was shown that Mlg_0216 exhibits both arsenate reductase and arsenite oxidase activities in vitro.…”

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confidence: 99%

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Identification of a Novel Arsenite Oxidase Gene, arxA , in the Haloalkaliphilic, Arsenite-Oxidizing Bacterium Alkalilimnicola ehrlichii Strain MLHE-1

et al. 2010

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Although arsenic is highly toxic to most organisms, certain prokaryotes are known to grow on and respire toxic metalloids of arsenic (i.e., arsenate and arsenite). Two enzymes are known to be required for this arsenic-based metabolism: (i) the arsenate respiratory reductase (ArrA) and (ii) arsenite oxidase (AoxB). Both catalytic enzymes contain molybdopterin cofactors and form distinct phylogenetic clades (ArrA and AoxB) within the dimethyl sulfoxide (DMSO) reductase family of enzymes. Here we report on the genetic identification of a "new" type of arsenite oxidase that fills a phylogenetic gap between the ArrA and AoxB clades of arsenic metabolic enzymes. This "new" arsenite oxidase is referred to as ArxA and was identified in the genome sequence of the Mono Lake isolate Alkalilimnicola ehrlichii MLHE-1, a chemolithoautotroph that can couple arsenite oxidation to nitrate reduction. A genetic system was developed for MLHE-1 and used to show that arxA (gene locus ID mlg_0216) was required for chemoautotrophic arsenite oxidation. Transcription analysis also showed that mlg_0216 was only expressed under anaerobic conditions in the presence of arsenite. The mlg_0216 gene is referred to as arxA because of its greater homology to arrA relative to aoxB and previous reports that implicated Mlg_0216 (ArxA) of MLHE-1 in reversible arsenite oxidation and arsenate reduction in vitro. Our results and past observations support the position that ArxA is a distinct clade within the DMSO reductase family of proteins. These results raise further questions about the evolutionary relationships between arsenite oxidases (AoxB) and arsenate respiratory reductases (ArrA).Arsenic is toxic to most organisms and is known to cause cancer in humans. However, bacteria have adapted several biotransformation pathways that function to either couple the reduction or oxidation of arsenicals to energy conservation and growth (1). The enzymologies of these two pathways have several features in common. The arsenate respiratory reductase (ArrAB) and arsenite oxidase (AoxAB) enzymes are usually composed of at least two subunits, a small iron-sulfur cluster-containing subunit (ArrB and AoxA) and a larger molybdopterin-containing catalytic subunit (ArrA and AoxB). Although they catalyze arsenic redox chemistry, ArrA and AoxB form distinct phylogenetic clades within the dimethyl sulfoxide (DMSO) reductase family of molybdenum-containing enzymes (16,24).Culture-dependent approaches have resulted in the isolation of a variety of diverse bacteria that metabolize arsenic (reviewed in reference 26). Many of these isolates have had their genomes sequenced, which has been insightful for understanding the composition and diversity of arr and aox gene clusters. In the arsenite-oxidizing nitrate reducer Alkalilimnicola ehrlichii strain MLHE-1 (a haloalkaliphile isolated from Mono Lake [CA]) (10, 15), bioinformatic analysis of its genome revealed the absence of genes homologous to the arsenite oxidase genes of the aoxB type. Instead, two genes (mlg_0216 and mlg_24...

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“…The ability of the same protein to catalyze both forward and reverse reactions is not without precedent. For example, haloalkaliphilic bacterial arsenate reductase can also function as an oxidase (Richey et al 2009). It is not yet clear if MsrA functions as an oxidase by a reversible covalent modification-induced conformational change and/or by interaction with a regulatory protein (Lim et al 2011).…”

Section: Met Oxidation Is Reversiblementioning

confidence: 99%

Convergent signaling pathways—interaction between methionine oxidation and serine/threonine/tyrosine O-phosphorylation

Rao

Thelen

Miernyk

2015

Cell Stress and Chaperones

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Oxidation of methionine (Met) to Met sulfoxide (MetSO) is a frequently found reversible posttranslational modification. It has been presumed that the major functional role for oxidation-labile Met residues is to protect proteins/ cells from oxidative stress. However, Met oxidation has been established as a key mechanism for direct regulation of a wide range of protein functions and cellular processes. Furthermore, recent reports suggest an interaction between Met oxidation and O-phosphorylation. Such interactions are a potentially direct interface between redox sensing and signaling, and cellular protein kinase/phosphatase-based signaling. Herein, we describe the current state of Met oxidation research, provide some mechanistic insight into crosstalk between these two major posttranslational modifications, and consider the evolutionary significance and regulatory potential of this crosstalk.

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Respiratory arsenate reductase as a bidirectional enzyme

Cited by 102 publications

References 30 publications

Unsuspected Diversity of Arsenite-Oxidizing Bacteria as Revealed by Widespread Distribution of theaoxBGene in Prokaryotes

Unsuspected Diversity of Arsenite-Oxidizing Bacteria as Revealed by Widespread Distribution of theaoxBGene in Prokaryotes

Identification of a Novel Arsenite Oxidase Gene, arxA , in the Haloalkaliphilic, Arsenite-Oxidizing Bacterium Alkalilimnicola ehrlichii Strain MLHE-1

Convergent signaling pathways—interaction between methionine oxidation and serine/threonine/tyrosine O-phosphorylation

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