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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.

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.

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Growth curves of GM1 grown at 4°C, 10°C and 20°C in the Minimal Salts Medium (MSM) with 0.04% (w/v) yeast extract. With 4 mM arsenite, closed circle; without arsenite, open circle; arsenite concentration, closed square. Error bars are the standard deviation of multiple experiments.
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Figure 3: Growth curves of GM1 grown at 4°C, 10°C and 20°C in the Minimal Salts Medium (MSM) with 0.04% (w/v) yeast extract. With 4 mM arsenite, closed circle; without arsenite, open circle; arsenite concentration, closed square. Error bars are the standard deviation of multiple experiments.

Mentions: Growth of GM1 was tested at 4°C, 10°C and 20°C in a minimal salts medium (MSM) with 0.04% (w/v) yeast extract in the presence and absence of 4 mM arsenite as described previously [15] (Note: GM1 was unable to grow chemolithoautotrophically with arsenite). Under all conditions arsenite was oxidised to arsenate and oxidation occurred in the early exponential phase of growth (Figure 3). The generation time of GM1 was shorter in the absence of arsenite, and decreased with increasing temperature (without arsenite at 4°C, 10°C and 20°C: 19 h, 16.5 h and 7 h, respectively; with arsenite at 4°C, 10°C and 20°C: 21.5 h, 17.7 h and 8.5 h, respectively). GM1 did not grow above 25°C. To date, only one arsenite oxidiser has been demonstrated to grow below 20°C [16]. This organism, a chemolithoautotrophic arsenite oxidiser designated M14, is a member of the Alphaproteobacteria related to Sinorhizobium species. M14's temperature range was between 10°C and 37°C with an optimum of 22°C [16]. GM1 is the first reported arsenite oxidiser capable of growth below 10°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)

Growth curves of GM1 grown at 4°C, 10°C and 20°C in the Minimal Salts Medium (MSM) with 0.04% (w/v) yeast extract. With 4 mM arsenite, closed circle; without arsenite, open circle; arsenite concentration, closed square. Error bars are the standard deviation of multiple experiments.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Growth curves of GM1 grown at 4°C, 10°C and 20°C in the Minimal Salts Medium (MSM) with 0.04% (w/v) yeast extract. With 4 mM arsenite, closed circle; without arsenite, open circle; arsenite concentration, closed square. Error bars are the standard deviation of multiple experiments.
Mentions: Growth of GM1 was tested at 4°C, 10°C and 20°C in a minimal salts medium (MSM) with 0.04% (w/v) yeast extract in the presence and absence of 4 mM arsenite as described previously [15] (Note: GM1 was unable to grow chemolithoautotrophically with arsenite). Under all conditions arsenite was oxidised to arsenate and oxidation occurred in the early exponential phase of growth (Figure 3). The generation time of GM1 was shorter in the absence of arsenite, and decreased with increasing temperature (without arsenite at 4°C, 10°C and 20°C: 19 h, 16.5 h and 7 h, respectively; with arsenite at 4°C, 10°C and 20°C: 21.5 h, 17.7 h and 8.5 h, respectively). GM1 did not grow above 25°C. To date, only one arsenite oxidiser has been demonstrated to grow below 20°C [16]. This organism, a chemolithoautotrophic arsenite oxidiser designated M14, is a member of the Alphaproteobacteria related to Sinorhizobium species. M14's temperature range was between 10°C and 37°C with an optimum of 22°C [16]. GM1 is the first reported arsenite oxidiser capable of growth below 10°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.

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