Earth Abides Arsenic Biotransformations

Abstract

Arsenic is the most prevalent environmental toxic element and causes health problems throughout the world. The toxicity, mobility, and fate of arsenic in the environment are largely determined by its speciation, and arsenic speciation changes are driven, at least to some extent, by biological processes. In this article, biotransformation of arsenic is reviewed from the perspective of the formation of Earth and the evolution of life, and the connection between arsenic geochemistry and biology is described. The article provides a comprehensive overview of molecular mechanisms of arsenic redox and methylation cycles as well as other arsenic biotransformations. It also discusses the implications of arsenic biotransformation in environmental remediation and food safety, with particular emphasis on groundwater arsenic contamination and arsenic accumulation in rice.

Keywords: MSMA; arsenic; degradation; methylation; oxidation; reduction; rice; roxarsone.

Figure 1

Stocks and fluxes of arsenic in various Earth components. Gray boxes indicate stocks of arsenic in a given component, and arrows indicate the fluxes of arsenic toward a given component. Data presented in this diagram are summarized from Wenzel (2013), in which detailed references are cited regarding the estimation of these stocks and fluxes.

Figure 2

Arsenic species and their biotransformations. Known enzymes for biotransformation are indicated in each step, and representative protein structures are shown for each enzyme: ArsC (Martin et al. 2001), AioAB (Ellis et al. 2001, Warelow et al. 2013), and ArsM (Ajees et al. 2012). Question marks indicate steps for which the molecular mechanism has yet to be unraveled. The diagram is partly adapted from Edmonds & Francesconi (1987).

Figure 3

Arsenic geothermal biology in Yellowstone National Park. Mats of Cyanidiales algae, which express the ArsM As(III) S-adenosylmethionine (SAM) methyltransferase, dominate the biomass in acidic geothermal outflow channels in (a) East Fork, Tantalus Creek, which drains the Norris Geyser Basin and (b) Nymph Creek, located in the Norris-Mammoth corridor in Yellowstone National Park. (c) Cyanidiales algae grow adjacent to realgar-like mineral phases and geothermal-derived waters containing 0.76 mM total arsenic. The orange-yellow deposits were determined by scanning electron microscope electron dispersive X-ray spectroscopy to be realgar-like, with an As:S ratio range of 1.1–1.3. Reproduced from Qin et al. (2009).

Figure 4

Arsenic biogeochemical cycles. Various microbial biotransformations of arsenic have roles in cycling of environmental arsenic between various chemical forms. As(V) and As(III) are interconverted by reduction (dark blue) and oxidation (red ), forming an arsenic redox cycle. Reduction of As(V) to As(III) is catalyzed by various microorganisms for arsenic detoxification or anaerobic arsenate respiration. The latter mechanism helps mobilize arsenic in the form of As(III) from As(V)-rich sediments and leads to arsenic contamination of groundwater and/or soil. As(III) is, in turn, oxidized back to As(V) by arsenite-oxidizing microbes. As(III) oxidation results in arsenic precipitation and adsorption to minerals in marine/freshwater sediments. Arsenite is also oxidized through arsenite-dependent anoxygenic photosynthesis. As an alternative detoxification process, arsenic is converted to mono-, di-, and trimethylated arsenicals (aqua). Methylation of arsenic also leads to volatilization of methylarsines, primarily trimethylarsine and some mono- and dimethylarsines (light blue). Inorganic and methylated arsenicals also form a bidirectional methylation cycle, wherein methylarsenicals are demethylated back to inorganic species (brown). Anthropogenic sources such as MAs(V) and roxarsone are also degraded into inorganic arsenicals in the environment and form a part of this cycle (white). In seawater, the major arsenic form As(V) is biotransformed into arsenosugar by algae, a process that is proposed to be completed by the combination of methylation and adenosylation ( gray). Arsenic accumulation is observed widely in many organisms ( purple). Ferns hyperaccumulate inorganic arsenic in above-ground tissues, and rice plants take up not only inorganic arsenic but also methylarsenicals and ultimately accumulate arsenic into the grain. Marine animals, in contrast, accumulate arsenosugar and arsenobetaine. Abbreviations: As(III), arsenite; As(V), arsenate; DMAs(V), dimethylarsenate; MAs(V), methylarsenate; Rox(V), roxarsone; TMAs(III), trimethylarsine; TMAs(V)O, trimethylarsine oxide.

Figure 5

Human exposure to groundwater arsenic through irrigation of rice paddy and drinking water. Arsenic from groundwater affects human health both directly (through drinking) and indirectly (through consuming rice irrigated with As-tainted groundwater). The pathway through rice was underestimated until recently (Zhu et al. 2008). Abbreviations: As(III), arsenite; As(V), arsenate; DMAs(III), dimethylarsenite; DMAs(V), dimethylarsenate; Me₂AsH, dimethylarsine; MAs(III), methylarsenite; MAs(V), methylarsenate; TMAs(III), trimethylarsine; TMAs(V)O, trimethylarsine oxide.