A Tale of Two Oxidation States: Bacterial Colonization of Arsenic-Rich Environments

Müller, Daniel J.; Médigue, Claudine; Koechler, Sandrine; Barbe, Valérie; Barakat, M.A.; Talla, Emmanuel; Bonnefoy, Violaine; Krin, Evelyne; Arsène-Ploetze, Florence; Carapito, Christine; Chandler, Michaël; Cournoyer, Benoît; Cruveiller, Stéphane; Dossat, Caroline; Duval, Simon; Heymann, Michaël; Leize, Emmanuelle; Lieutaud, Aurélie; Lièvremont, Didier; Makita, Yuko; Mangenot, Sophie; Nitschke, Wolfgang; Ortet, Philippe; Perdrial, Nicolas; Schoepp, Barbara; Siguier, Patricia; Simeonova, Diliana D.; Rouy, Zoé; Ségurens, Béatrice; Turlin, Évelyne; Vallenet, David; Dorsselaer, Alain Van; Weiss, Stéphanie; Weissenbach, Jean; Lett, Marie‐Claire; Danchin, Antoine; Bertin, Philippe

doi:10.1371/journal.pgen.0030053.eor

Cited by 15 publications

(34 citation statements)

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“…In the last few years, a huge amount of genomic sequences have been published in databases, including a complete characterization of several bacteria metabolizing arsenic (Muller et al, 2007;Arsène-Ploetze et al, 2010). In microbial ecology, the major challenge remains, however, to determine more precisely the role of microorganisms and their relationships with other members of the microbial community that result in an efficient functioning of the ecosystem.…”

Section: Discussionmentioning

confidence: 99%

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Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics

et al. 2011

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By their metabolic activities, microorganisms have a crucial role in the biogeochemical cycles of elements. The complete understanding of these processes requires, however, the deciphering of both the structure and the function, including synecologic interactions, of microbial communities. Using a metagenomic approach, we demonstrated here that an acid mine drainage highly contaminated with arsenic is dominated by seven bacterial strains whose genomes were reconstructed. Five of them represent yet uncultivated bacteria and include two strains belonging to a novel bacterial phylum present in some similar ecosystems, and which was named 'Candidatus Fodinabacter communificans.' Metaproteomic data unravelled several microbial capabilities expressed in situ, such as iron, sulfur and arsenic oxidation that are key mechanisms in biomineralization, or organic nutrient, amino acid and vitamin metabolism involved in synthrophic associations. A statistical analysis of genomic and proteomic data and reverse transcriptase-PCR experiments allowed us to build an integrated model of the metabolic interactions that may be of prime importance in the natural attenuation of such anthropized ecosystems.

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Section: Discussionmentioning

confidence: 99%

“…Nebulized DNA fragments ranging from 3 to 5 kb were used to construct a genomic library and DNA inserts were sequenced, as previously described (Muller et al, 2007), giving rise to 550 920 Sanger reads. In parallel, 281 758 DNA reads were obtained by GS-FLEX pyrosequencing using standard procedures.…”

Section: Methodsmentioning

confidence: 99%

Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics

et al. 2011

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“…In MLHE-1, putative regulators (encoded by mlg_0218-0220) of the arx operon are located adjacent and in the opposite orientation to arxBЈABCDE. These putative regulators include a periplasmic phosphonate binding protein (Mlg_0218), a two-component signal transduction histidine ki- tumefaciens and other arsenite oxidizers (12,23). Aerobic/anaerobic conditions were also a primary factor that led to the differential expression of arxA.…”

Section: Discussionmentioning

confidence: 99%

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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“…SY8 strain (Cai et al, 2009). Homologs of the aioSR (twocomponent signal-transduction system) and aioAB (arsenite oxidase) genes are also present in the aio/aox loci of Herminiimonas arsenicoxydans (Muller et al, 2007) and Alcaligenes faecalis (Silver and Phung 2005a), but the regulatory genes (aioSR/aoxSR) in these hosts are separated from the structural genes (aioAB) by an additional ORF.…”

Section: Arsenic Metabolism and Resistance Gene Islandmentioning

confidence: 99%

Structural and functional genomics of plasmid pSinA of Sinorhizobium sp. M14 encoding genes for the arsenite oxidation and arsenic resistance

Drewniak

Dziewit

Ciezkowska

et al. 2013

Journal of Biotechnology

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Plasmid pSinA of Sinorhizobium sp. M14 (Alphaproteobacteria) is the first described, natural, self-transferable plasmid harboring a complete set of genes for oxidation of arsenite. Removal of this plasmid from cells of the host strain caused the loss of resistance to arsenic and heavy metals (Cd, Co, Zn and Hg) and abolished the ability to grow on minimal salt medium supplemented with sodium arsenite as the sole energy source. Plasmid pSinA was introduced into other representatives of Alphaproteobacteria which resulted in acquisition of new abilities concerning arsenic resistance and oxidation, as well as heavy metals resistance. Microcosm experiments revealed that plasmid pSinA can also be transferred via conjugation into other indigenous bacteria from microbial community of As-contaminated soils, including representatives of Alpha-and Gammaproteobacteria. Analysis of "natural" transconjugants showed that pSinA is functional (expresses arsenite oxidase) and is stably maintained in their cells after approximately 60 generations of growth under nonselective conditions. This work clearly demonstrates that pSinA is a self-transferable, broad-host-range plasmid, which plays an important role in horizontal transfer of arsenic metabolism genes.

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A Tale of Two Oxidation States: Bacterial Colonization of Arsenic-Rich Environments

Cited by 15 publications

References 0 publications

Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics

Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics

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

Structural and functional genomics of plasmid pSinA of Sinorhizobium sp. M14 encoding genes for the arsenite oxidation and arsenic resistance

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