Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga

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.arsenic detoxification ͉ arsenic methylation ͉ As(III) S-adenosylmethyltransferase ͉ thermophile

Arsenic methylation by an arsenite S-adenosylmethionine methyltransferase from Spirulina platensis

“…Arsenic is ubiquitous in aquatic environments where various kinds of cyanobacteria are distributed (Qin et al, 2006(Qin et al, , 2009Zhang et al, 2013), so cyanobacteria have evolved several ways to detoxify As in order to survive in the environment (Aurilio et al, 1994;Knauer et al, 1999). In this study, our results showed that S. platensis could grow at high concentrations of the toxic metalloid and had the capability of As(III) accumulation and biotransformation.…”

“…The huge difference between the sequences may explain the difference in methylation products. In addition, As(III) was seen to be transformed to DMA(V) within 30 min, and the catalytic rate of SpArsM was much faster than that of other ArsMs (Qin et al, 2009;Wang et al, 2014a;Zhang et al, 2015). Meanwhile, the intermediate MMA(III) and MMA(V) were absent in the in vitro enzyme activity assays when the reaction was performed at optimal conditions, and only MMA(V) was observed when the enzyme was impaired, for example under higher or lower temperature.…”

Cyanobacteria produce arsenosugars

“…PCC 7120 incorporate As into sugars as Oxo-Gly and Oxo-PO 4 . This is the first report clearly demonstrating that cyanobacteria have an ability to produce arsenosugars, which could well have important implications for freshwater lakes and hot springs occurring in the vicinity of soils rich in As (there is in fact a report of arsenosugars in hotspring mats [38] ).…”

A C⋅As lyase for degradation of environmental organoarsenical herbicides and animal husbandry growth promoters

“…These biotransformations include redox cycles between the relatively innocuous pentavalent arsenate and the considerably more toxic and carcinogenic trivalent arsenite (2,3). In addition, many microbes, both prokaryotic and eukaryotic, have arsM genes for inorganic arsenite [As(III)] S-adenosylmethionine methyltransferases that methylate inorganic As(III) to mono-, di-, and tri-methylated species (4,5). The genes encoding arsenic transforming enzymes are widely distributed, and these arsenic biotransformations have been proposed to play significant roles in the arsenic biogeocycle and in remodeling the terrain in volcanic areas such as Yellowstone National Park and regions of the world with high amounts of arsenic in soil and water such as West Bengal and Bangladesh (3,6).…”