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Microbial oxidation of arsenite in a subarctic environment: diversity of arsenite oxidase genes and identification of a psychrotolerant arsenite oxidiser.

Osborne TH, Jamieson HE, Hudson-Edwards KA, Nordstrom DK, Walker SR, Ward SA, Santini JM - BMC Microbiol. (2010)

Bottom Line: No arsenic metabolism (either dissimilatory arsenate reduction or arsenite oxidation) has ever been reported in cold environments (i.e. < 10 degrees C).We compared the arsenite oxidisers in two subsamples (which differed in arsenite concentration) collected from one biofilm. 'Species' (sequence) richness did not differ between subsamples, but the relative importance of the three identifiable clades did.The diversity of arsenite oxidisers does not significantly differ from two subsamples of a microbial biofilm that vary in arsenite concentrations.

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Affiliation: Institute of Structural and Molecular Biology, UCL, Darwin Building, London, UK.

ABSTRACT

Background: Arsenic is toxic to most living cells. The two soluble inorganic forms of arsenic are arsenite (+3) and arsenate (+5), with arsenite the more toxic. Prokaryotic metabolism of arsenic has been reported in both thermal and moderate environments and has been shown to be involved in the redox cycling of arsenic. No arsenic metabolism (either dissimilatory arsenate reduction or arsenite oxidation) has ever been reported in cold environments (i.e. < 10 degrees C).

Results: Our study site is located 512 kilometres south of the Arctic Circle in the Northwest Territories, Canada in an inactive gold mine which contains mine waste water in excess of 50 mM arsenic. Several thousand tonnes of arsenic trioxide dust are stored in underground chambers and microbial biofilms grow on the chamber walls below seepage points rich in arsenite-containing solutions. We compared the arsenite oxidisers in two subsamples (which differed in arsenite concentration) collected from one biofilm. 'Species' (sequence) richness did not differ between subsamples, but the relative importance of the three identifiable clades did. An arsenite-oxidising bacterium (designated GM1) was isolated, and was shown to oxidise arsenite in the early exponential growth phase and to grow at a broad range of temperatures (4-25 degrees C). Its arsenite oxidase was constitutively expressed and functioned over a broad temperature range.

Conclusions: The diversity of arsenite oxidisers does not significantly differ from two subsamples of a microbial biofilm that vary in arsenite concentrations. GM1 is the first psychrotolerant arsenite oxidiser to be isolated with the ability to grow below 10 degrees C. This ability to grow at low temperatures could be harnessed for arsenic bioremediation in moderate to cold climates.

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Specific activity of GM1 arsenite oxidase as a function of temperature. Error bars are the standard deviation of multiple assays.
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Figure 4: Specific activity of GM1 arsenite oxidase as a function of temperature. Error bars are the standard deviation of multiple assays.

Mentions: In most cases, arsenite is required in the growth medium for arsenite oxidase gene expression [6]. There are two exceptions, Thiomonas sp. str. 3As and Agrobacterium tumefaciens str. 5A, where the arsenite oxidase is expressed when the organisms are grown in the absence of arsenite but in the latter the expression does not occur until stationary phase [17,18]. In GM1 arsenite oxidase expression is also constitutive when grown in the absence of arsenite [i.e. in the MSM with 0.04% (w/v) yeast extract] with 0.367 U/mg observed in late exponential phase and activity also detected in early exponential phase (0.13 U/mg). Taken together this information suggests that there are at least two modes of regulating the expression of the aro genes in GM1, possibly a two-component signal transduction system and quorum sensing. Because of the broad temperature range for growth of GM1, arsenite oxidase activity was determined at a variety of temperatures (Figure 4). Activity occurred over a broad temperature range reaching a maximum at temperatures well above the optimum for growth (i.e. between 40-50°C).


Microbial oxidation of arsenite in a subarctic environment: diversity of arsenite oxidase genes and identification of a psychrotolerant arsenite oxidiser.

Osborne TH, Jamieson HE, Hudson-Edwards KA, Nordstrom DK, Walker SR, Ward SA, Santini JM - BMC Microbiol. (2010)

Specific activity of GM1 arsenite oxidase as a function of temperature. Error bars are the standard deviation of multiple assays.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2921403&req=5

Figure 4: Specific activity of GM1 arsenite oxidase as a function of temperature. Error bars are the standard deviation of multiple assays.
Mentions: In most cases, arsenite is required in the growth medium for arsenite oxidase gene expression [6]. There are two exceptions, Thiomonas sp. str. 3As and Agrobacterium tumefaciens str. 5A, where the arsenite oxidase is expressed when the organisms are grown in the absence of arsenite but in the latter the expression does not occur until stationary phase [17,18]. In GM1 arsenite oxidase expression is also constitutive when grown in the absence of arsenite [i.e. in the MSM with 0.04% (w/v) yeast extract] with 0.367 U/mg observed in late exponential phase and activity also detected in early exponential phase (0.13 U/mg). Taken together this information suggests that there are at least two modes of regulating the expression of the aro genes in GM1, possibly a two-component signal transduction system and quorum sensing. Because of the broad temperature range for growth of GM1, arsenite oxidase activity was determined at a variety of temperatures (Figure 4). Activity occurred over a broad temperature range reaching a maximum at temperatures well above the optimum for growth (i.e. between 40-50°C).

Bottom Line: No arsenic metabolism (either dissimilatory arsenate reduction or arsenite oxidation) has ever been reported in cold environments (i.e. < 10 degrees C).We compared the arsenite oxidisers in two subsamples (which differed in arsenite concentration) collected from one biofilm. 'Species' (sequence) richness did not differ between subsamples, but the relative importance of the three identifiable clades did.The diversity of arsenite oxidisers does not significantly differ from two subsamples of a microbial biofilm that vary in arsenite concentrations.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Structural and Molecular Biology, UCL, Darwin Building, London, UK.

ABSTRACT

Background: Arsenic is toxic to most living cells. The two soluble inorganic forms of arsenic are arsenite (+3) and arsenate (+5), with arsenite the more toxic. Prokaryotic metabolism of arsenic has been reported in both thermal and moderate environments and has been shown to be involved in the redox cycling of arsenic. No arsenic metabolism (either dissimilatory arsenate reduction or arsenite oxidation) has ever been reported in cold environments (i.e. < 10 degrees C).

Results: Our study site is located 512 kilometres south of the Arctic Circle in the Northwest Territories, Canada in an inactive gold mine which contains mine waste water in excess of 50 mM arsenic. Several thousand tonnes of arsenic trioxide dust are stored in underground chambers and microbial biofilms grow on the chamber walls below seepage points rich in arsenite-containing solutions. We compared the arsenite oxidisers in two subsamples (which differed in arsenite concentration) collected from one biofilm. 'Species' (sequence) richness did not differ between subsamples, but the relative importance of the three identifiable clades did. An arsenite-oxidising bacterium (designated GM1) was isolated, and was shown to oxidise arsenite in the early exponential growth phase and to grow at a broad range of temperatures (4-25 degrees C). Its arsenite oxidase was constitutively expressed and functioned over a broad temperature range.

Conclusions: The diversity of arsenite oxidisers does not significantly differ from two subsamples of a microbial biofilm that vary in arsenite concentrations. GM1 is the first psychrotolerant arsenite oxidiser to be isolated with the ability to grow below 10 degrees C. This ability to grow at low temperatures could be harnessed for arsenic bioremediation in moderate to cold climates.

Show MeSH