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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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Circular Representation of H. arsenicoxydans GenomeCircles 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.
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pgen-0030053-g001: Circular Representation of H. arsenicoxydans GenomeCircles 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.

Mentions: The H. arsenicoxydans genome consists of a single circular chromosome of 3,424,307 bp (Figure 1) with a total of 3,333 coding sequences (CDSs), among which 38% are of unknown function (Table 1). Surprisingly, any attempt to identify extrachromosomal elements in this strain by DNA sequencing, pulse-field electrophoresis, or plasmid purification was unsuccessful (unpublished data). This suggests that, unlike many microbes isolated from natural or anthropized environments, H. arsenicoxydans contains neither a second chromosome nor a (mega)plasmid. In bacteria, mobile genetic elements are known to play a major role in the acquisition of genes involved in adaptation to environmental stresses [17]. In line with this observation and in contrast to the situation in related microorganisms such as Ralstonia metallidurans [18], only a small number of complete or partial insertion sequences (IS) were identified in the genome of H. arsenicoxydans (Table S1). These IS elements represent 0.65% of the genome and belong to several families; i.e., IS3, IS30, and IS110. H. arsenicoxydans also contains more complex transposons or transposon remnants, but, unlike those identified in biomining strains used for metal recovery from gold-bearing arsenopyrite ores [19], they do not convincingly harbor arsenic-resistance determinants. Interestingly, all the complete ISs are inserted with their transposase genes in a clockwise orientation with respect to the orientation of the replication fork, suggesting some sort of interference between replication and IS stability.


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)

Circular Representation of H. arsenicoxydans GenomeCircles 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.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0030053-g001: Circular Representation of H. arsenicoxydans GenomeCircles 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.
Mentions: The H. arsenicoxydans genome consists of a single circular chromosome of 3,424,307 bp (Figure 1) with a total of 3,333 coding sequences (CDSs), among which 38% are of unknown function (Table 1). Surprisingly, any attempt to identify extrachromosomal elements in this strain by DNA sequencing, pulse-field electrophoresis, or plasmid purification was unsuccessful (unpublished data). This suggests that, unlike many microbes isolated from natural or anthropized environments, H. arsenicoxydans contains neither a second chromosome nor a (mega)plasmid. In bacteria, mobile genetic elements are known to play a major role in the acquisition of genes involved in adaptation to environmental stresses [17]. In line with this observation and in contrast to the situation in related microorganisms such as Ralstonia metallidurans [18], only a small number of complete or partial insertion sequences (IS) were identified in the genome of H. arsenicoxydans (Table S1). These IS elements represent 0.65% of the genome and belong to several families; i.e., IS3, IS30, and IS110. H. arsenicoxydans also contains more complex transposons or transposon remnants, but, unlike those identified in biomining strains used for metal recovery from gold-bearing arsenopyrite ores [19], they do not convincingly harbor arsenic-resistance determinants. Interestingly, all the complete ISs are inserted with their transposase genes in a clockwise orientation with respect to the orientation of the replication fork, suggesting some sort of interference between replication and IS stability.

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