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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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Effect of Metal and Metalloid Concentration on Swimming Properties in H. arsenicoxydansMotility assays were performed in the presence of an increasing concentration of As[III], Co[II], or Fe[III]. The level of motility of ULPAs wild-type strain and of its aoxAB knockout derivative was evaluated as the diameter of the swimming ring expressed in millimeters. The results are the mean value of three independent experiments.
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pgen-0030053-g006: Effect of Metal and Metalloid Concentration on Swimming Properties in H. arsenicoxydansMotility assays were performed in the presence of an increasing concentration of As[III], Co[II], or Fe[III]. The level of motility of ULPAs wild-type strain and of its aoxAB knockout derivative was evaluated as the diameter of the swimming ring expressed in millimeters. The results are the mean value of three independent experiments.

Mentions: Although the flagellum morphology was not affected by the presence of arsenic (Figure S5), at least with respect to length and width, an increased concentration of this toxic element resulted in a concomitant increase in bacterial motility on semisolid agar plates (Figure 6) and in flagellar gene expression (Table 2). Aside from iron, an element that is essential to life, no such effect occurred with other toxic elements tested, such as Co[II] (Figure 6), Cu[II], Sb[III], or As[V] (unpublished data). The hypothesis that arsenic contributes to the metabolism of H. arsenicoxydans was further supported by the positive chemotactic response shown by the strain towards As[III] (Figure 7A). This observation suggests that the bacterium is able to sense and respond to the presence of As[III] in the medium. The genome of H. arsenicoxydans contains 12 methyl-accepting chemotaxis proteins–encoding genes. As most of these genes have no predicted function, it is tempting to speculate that at least one of them plays a role in this mechanism.


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)

Effect of Metal and Metalloid Concentration on Swimming Properties in H. arsenicoxydansMotility assays were performed in the presence of an increasing concentration of As[III], Co[II], or Fe[III]. The level of motility of ULPAs wild-type strain and of its aoxAB knockout derivative was evaluated as the diameter of the swimming ring expressed in millimeters. The results are the mean value of three independent experiments.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0030053-g006: Effect of Metal and Metalloid Concentration on Swimming Properties in H. arsenicoxydansMotility assays were performed in the presence of an increasing concentration of As[III], Co[II], or Fe[III]. The level of motility of ULPAs wild-type strain and of its aoxAB knockout derivative was evaluated as the diameter of the swimming ring expressed in millimeters. The results are the mean value of three independent experiments.
Mentions: Although the flagellum morphology was not affected by the presence of arsenic (Figure S5), at least with respect to length and width, an increased concentration of this toxic element resulted in a concomitant increase in bacterial motility on semisolid agar plates (Figure 6) and in flagellar gene expression (Table 2). Aside from iron, an element that is essential to life, no such effect occurred with other toxic elements tested, such as Co[II] (Figure 6), Cu[II], Sb[III], or As[V] (unpublished data). The hypothesis that arsenic contributes to the metabolism of H. arsenicoxydans was further supported by the positive chemotactic response shown by the strain towards As[III] (Figure 7A). This observation suggests that the bacterium is able to sense and respond to the presence of As[III] in the medium. The genome of H. arsenicoxydans contains 12 methyl-accepting chemotaxis proteins–encoding genes. As most of these genes have no predicted function, it is tempting to speculate that at least one of them plays a role in this mechanism.

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