Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga

TLDR

Arsenic is the most common environmental toxin, especially abundant in geothermal settings where microbial redox transformations occur, yet eukaryotic contributions have been largely overlooked. The study investigates whether a thermophilic eukaryotic alga of the Cyanidiales order can mediate arsenic cycling at elevated temperatures. The Cyanidioschyzon sp. isolate 5508 oxidizes arsenite to arsenate, reduces arsenate back to arsenite, and methylates arsenite to produce TMAO and DMAs(V); two cloned methyltransferase genes, CmarsM7 and CmarsM8, confer As(III) resistance when expressed in *E.

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 T opt 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.