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A tale of two oxidation states: bacterial colonization of arsenic-rich environments.

Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, Van Dorsselaer A, Weiss S, Weissenbach J, Lett MC, Danchin A, Bertin PN - PLoS Genet. (2007)

Bottom Line: Although this metalloid is ubiquitous on Earth, thus far no bacterium thriving in arsenic-contaminated environments has been fully characterized.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.

View Article: PubMed Central - PubMed

Affiliation: Génétique Moléculaire, Génomique et Microbiologie, UMR7156 CNRS and Université Louis Pasteur, Strasbourg, France.

ABSTRACT
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 beta-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.

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Detailed View of a GC-Rich IslandThe chromosomal segment extends between positions 1.97 and 2.07 Mb on the H. arsenicoxydans chromosome. Frames display (from top to bottom): (1) %GC along this island; (2) annotated CDSs on the direct (D) and reverse (R) strand: arsIII gene cluster (six genes in red arrows), part of the clc element of plasmid (or phage) origin, initially described in Pseudomonas sp. strain B13 [22] (64 genes in light blue arrows), and phage-related function (DNA repair, integrase) associated with metabolic capabilities, such as formaldelyde oxidation (17 genes in light green arrows), small genes are represented by a line; (3) synteny maps, calculated on a set of selected genomes (RALME, Ralstonia metallidurans CH34; BURXE, Burkholderia xenovorans LB400; AZOSE, Azoarcus sp. EbN1; PSEF5, Pseudomonas fluorescens Pf-5; and XANAC, Xanthomonas campestris 85–10). A line contains the similarity results between H. arsenicoxydans and one given genome. A rectangle represents a putative ortholog between one CDS of the compared genome and the CDS of the H. arsenicoxydans genome opposite. When, for several CDSs colocalized on the H. arsenicoxydans genome, several colocalized orthologs have been identified in the compared genome, the rectangles will be of the same color. Otherwise, the rectangle is white. A group of rectangles of the same color therefore indicates the existence of a synteny between H. arsenicoxydans and the compared genome, using a gap parameters of five genes maximum [63]. Details on correspondences between genes in the synteny (Table S2) show that the light blue section of this island in H. arsenicoxydans is also found at the same chromosomal location in the compared genomes.
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pgen-0030053-g002: Detailed View of a GC-Rich IslandThe chromosomal segment extends between positions 1.97 and 2.07 Mb on the H. arsenicoxydans chromosome. Frames display (from top to bottom): (1) %GC along this island; (2) annotated CDSs on the direct (D) and reverse (R) strand: arsIII gene cluster (six genes in red arrows), part of the clc element of plasmid (or phage) origin, initially described in Pseudomonas sp. strain B13 [22] (64 genes in light blue arrows), and phage-related function (DNA repair, integrase) associated with metabolic capabilities, such as formaldelyde oxidation (17 genes in light green arrows), small genes are represented by a line; (3) synteny maps, calculated on a set of selected genomes (RALME, Ralstonia metallidurans CH34; BURXE, Burkholderia xenovorans LB400; AZOSE, Azoarcus sp. EbN1; PSEF5, Pseudomonas fluorescens Pf-5; and XANAC, Xanthomonas campestris 85–10). A line contains the similarity results between H. arsenicoxydans and one given genome. A rectangle represents a putative ortholog between one CDS of the compared genome and the CDS of the H. arsenicoxydans genome opposite. When, for several CDSs colocalized on the H. arsenicoxydans genome, several colocalized orthologs have been identified in the compared genome, the rectangles will be of the same color. Otherwise, the rectangle is white. A group of rectangles of the same color therefore indicates the existence of a synteny between H. arsenicoxydans and the compared genome, using a gap parameters of five genes maximum [63]. Details on correspondences between genes in the synteny (Table S2) show that the light blue section of this island in H. arsenicoxydans is also found at the same chromosomal location in the compared genomes.

Mentions: Circles display (from the outside inward): (rings 1 and 2) predicted CDSs transcribed in a clockwise/counterclockwise direction, (ring 3) tRNA (green) and rRNA (violetblue), (ring 4) ISs (yellow) and prophagic regions (violetbrown), (ring 5) clusters of genes involved in arsenic (red; numbered as shown in Figure 4)/metal resistance (dark blue), (ring 6) GC deviation (GCwindow − average GC of genome, using a 1kb window); (7) GC skew (using a 1kb window). The high GC-rich island described in Figure 2 is shown in red.


A tale of two oxidation states: bacterial colonization of arsenic-rich environments.

Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, Van Dorsselaer A, Weiss S, Weissenbach J, Lett MC, Danchin A, Bertin PN - PLoS Genet. (2007)

Detailed View of a GC-Rich IslandThe chromosomal segment extends between positions 1.97 and 2.07 Mb on the H. arsenicoxydans chromosome. Frames display (from top to bottom): (1) %GC along this island; (2) annotated CDSs on the direct (D) and reverse (R) strand: arsIII gene cluster (six genes in red arrows), part of the clc element of plasmid (or phage) origin, initially described in Pseudomonas sp. strain B13 [22] (64 genes in light blue arrows), and phage-related function (DNA repair, integrase) associated with metabolic capabilities, such as formaldelyde oxidation (17 genes in light green arrows), small genes are represented by a line; (3) synteny maps, calculated on a set of selected genomes (RALME, Ralstonia metallidurans CH34; BURXE, Burkholderia xenovorans LB400; AZOSE, Azoarcus sp. EbN1; PSEF5, Pseudomonas fluorescens Pf-5; and XANAC, Xanthomonas campestris 85–10). A line contains the similarity results between H. arsenicoxydans and one given genome. A rectangle represents a putative ortholog between one CDS of the compared genome and the CDS of the H. arsenicoxydans genome opposite. When, for several CDSs colocalized on the H. arsenicoxydans genome, several colocalized orthologs have been identified in the compared genome, the rectangles will be of the same color. Otherwise, the rectangle is white. A group of rectangles of the same color therefore indicates the existence of a synteny between H. arsenicoxydans and the compared genome, using a gap parameters of five genes maximum [63]. Details on correspondences between genes in the synteny (Table S2) show that the light blue section of this island in H. arsenicoxydans is also found at the same chromosomal location in the compared genomes.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1851979&req=5

pgen-0030053-g002: Detailed View of a GC-Rich IslandThe chromosomal segment extends between positions 1.97 and 2.07 Mb on the H. arsenicoxydans chromosome. Frames display (from top to bottom): (1) %GC along this island; (2) annotated CDSs on the direct (D) and reverse (R) strand: arsIII gene cluster (six genes in red arrows), part of the clc element of plasmid (or phage) origin, initially described in Pseudomonas sp. strain B13 [22] (64 genes in light blue arrows), and phage-related function (DNA repair, integrase) associated with metabolic capabilities, such as formaldelyde oxidation (17 genes in light green arrows), small genes are represented by a line; (3) synteny maps, calculated on a set of selected genomes (RALME, Ralstonia metallidurans CH34; BURXE, Burkholderia xenovorans LB400; AZOSE, Azoarcus sp. EbN1; PSEF5, Pseudomonas fluorescens Pf-5; and XANAC, Xanthomonas campestris 85–10). A line contains the similarity results between H. arsenicoxydans and one given genome. A rectangle represents a putative ortholog between one CDS of the compared genome and the CDS of the H. arsenicoxydans genome opposite. When, for several CDSs colocalized on the H. arsenicoxydans genome, several colocalized orthologs have been identified in the compared genome, the rectangles will be of the same color. Otherwise, the rectangle is white. A group of rectangles of the same color therefore indicates the existence of a synteny between H. arsenicoxydans and the compared genome, using a gap parameters of five genes maximum [63]. Details on correspondences between genes in the synteny (Table S2) show that the light blue section of this island in H. arsenicoxydans is also found at the same chromosomal location in the compared genomes.
Mentions: Circles display (from the outside inward): (rings 1 and 2) predicted CDSs transcribed in a clockwise/counterclockwise direction, (ring 3) tRNA (green) and rRNA (violetblue), (ring 4) ISs (yellow) and prophagic regions (violetbrown), (ring 5) clusters of genes involved in arsenic (red; numbered as shown in Figure 4)/metal resistance (dark blue), (ring 6) GC deviation (GCwindow − average GC of genome, using a 1kb window); (7) GC skew (using a 1kb window). The high GC-rich island described in Figure 2 is shown in red.

Bottom Line: Although this metalloid is ubiquitous on Earth, thus far no bacterium thriving in arsenic-contaminated environments has been fully characterized.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.

View Article: PubMed Central - PubMed

Affiliation: Génétique Moléculaire, Génomique et Microbiologie, UMR7156 CNRS and Université Louis Pasteur, Strasbourg, France.

ABSTRACT
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 beta-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.

Show MeSH
Related in: MedlinePlus