Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga
- Jie Qina,1,
- Corinne R. Lehrb,2,
- Chungang Yuanc,d,
- X. Chris Lec,
- Timothy R. McDermottb and
- Barry P. Rosena,13
- aDepartment of Biochemistry and Molecular Biology, Wayne State University School of Medicine, Detroit, MI 48201;
- bDepartment of Land Resources and Environmental Sciences and Thermal Biology Institute, Montana State University, Bozeman, MT 59717;
- cAnalytical and Environmental Toxicology, Department of Laboratory Medicine and Pathology, University of Alberta, Edmonton, AB, Canada T6G 2G3; and
- dSchool of Environmental Science and Engineering, North China Electric Power University, Baoding 071003, Hebei Province, People's Republic of China
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Edited by Peter C. Agre, Johns Hopkins University, Baltimore, MD, and approved February 6, 2009 (received for review January 10, 2009)
Abstract
Arsenic is the most common toxic substance in the environment, ranking first on the Superfund list of hazardous substances. It is introduced primarily from geochemical sources and is acted on biologically, creating an arsenic biogeocycle. Geothermal environments are known for their elevated arsenic content and thus provide an excellent setting in which to study microbial redox transformations of arsenic. To date, most studies of microbial communities in geothermal environments have focused on Bacteria and Archaea, with little attention to eukaryotic microorganisms. Here, we show the potential of an extremophilic eukaryotic alga of the order Cyanidiales to influence arsenic cycling at elevated temperatures. Cyanidioschyzon sp. isolate 5508 oxidized arsenite [As(III)] to arsenate [As(V)], reduced As(V) to As(III), and methylated As(III) to form trimethylarsine oxide (TMAO) and dimethylarsenate [DMAs(V)]. Two arsenic methyltransferase genes, CmarsM7 and CmarsM8, were cloned from this organism and demonstrated to confer resistance to As(III) in an arsenite hypersensitive strain of Escherichia coli. The 2 recombinant CmArsMs were purified and shown to transform As(III) into monomethylarsenite, DMAs(V), TMAO, and trimethylarsine gas, with a Topt of 60–70 °C. These studies illustrate the importance of eukaryotic microorganisms to the biogeochemical cycling of arsenic in geothermal systems, offer a molecular explanation for how these algae tolerate arsenic in their environment, and provide the characterization of algal methyltransferases.
Footnotes
- 3To whom correspondence should be addressed. E-mail: brosen{at}fiu.edu
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Author contributions: J.Q., T.R.M., and B.P.R. designed research; J.Q., C.R.L., C.Y., and T.R.M. performed research; C.Y. and X.C.L. contributed new reagents/analytic tools; X.C.L., T.R.M., and B.P.R. analyzed data; and J.Q., T.R.M., and B.P.R. wrote the paper.
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↵1Present address: Department of Cellular Biology, Florida International University College of Medicine, Miami, FL 33199.
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↵2Present address: Department of Chemistry and Biochemistry, California Polytechnic State University, San Luis Obispo, CA 93407.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
