Toxicity mechanisms of arsenic compounds in aquatic organisms

Highlights

• Arsenic (As) is a toxic metalloid that is widely distributed in the environment.

• Arsenic toxicity is highly diverse and complex depending on its chemical form.

• As toxicity is mainly associated with oxidative stress mechanisms.

• AQP, HXT, phosphate channels, and ABC are involved in As influx/efflux systems.

• Freshwater and marine organisms have As-specific biotransformation systems.

Abstract

Arsenic is a toxic metalloid that is widely distributed in the environment due to its persistence and accumulative properties. The occurrence, distribution, and biological effects of arsenic in aquatic environments have been extensively studied. Acute and chronic toxicities to arsenic are associated with fatal effects at the individual and molecular levels. The toxicity of arsenic in aquatic organisms depends on its speciation and concentration. In aquatic environments, inorganic arsenic is the dominant form. While trivalent arsenicals have greater toxicity compared with pentavalent arsenicals, inorganic arsenic can assume a variety of forms through biotransformation in aquatic organisms. Biotransformation mechanisms and speciation of arsenic have been studied, but few reports have addressed the relationships among speciation, toxicity, and bioavailability in biological systems. This paper reviews the modes of action of arsenic along with its toxic effects and distribution in an attempt to improve our understanding of the mechanisms of arsenic toxicity in aquatic organisms.

Introduction

Arsenic is a crystalline metalloid possessing properties of both metallic and non-metallic elements that is widely distributed in natural environments. It is the 20th most abundant element on the Earth's crust and the 14th most abundant in seawater (National Research Council, 1977; Mandal et al., 2002; Garelick et al., 2008). Natural sources such as volcanic eruptions contribute to arsenic pollution, and human activities (e.g., manufacturing of alloys, glass, pesticides, and pharmaceutical products) also cause environmental accumulation of arsenic (Cubadda et al., 2010). Arsenic from natural and anthropogenic sources is discharged into the atmosphere, groundwater, and rivers and ultimately flows into the ocean. Arsenic concentrations in freshwater and seawater are typically less than 10 µg/L (Rahman and Hasegawa, 2012) and 1.5 µg/L (Smedley and Kinniburgh, 2002), respectively. However, in some areas, high concentrations have been reported, ranging from 0.5-5,000 µg/L in drinking water under polluted conditions (Mandal and Suzuki, 2002). Concentrations of 1,100 µg/L arsenic were reportedly found downstream of an industrial arsenic-producing complex in South Carolina (Smedley and Kinniburgh, 2001).

Arsenic contamination can be absorbed by aquatic organisms via ingestion, inhalation, and/or permeation of the skin or mucous membranes, entering cells through active transport (Yang et al., 2012; Hong et al., 2014). Absorbed arsenic can cause adverse biochemical and physiological effects such as poisoning, reduced reproduction and growth, immune disorders, cell and tissue damage, and cell death in aquatic organisms (Table 1). The toxic effects of arsenic vary by chemical form. Arsenic exists in four oxidation states: arsenate (As^V), arsenite (As^III), arsenic (As), and arsine (As^−III) (Sharma and Sohn, 2009). Inorganic arsenic (iAs), As^V and As^III, are dominant forms in aquatic environments, while elemental arsenic is rare, and As^−III is present only in extremely reduced environments with a low redox potential (Neff, 1997). In general, organometallic compounds are more toxic than inorganic metals (Prange and Jantzen, 1995). However, due to higher solubility of iAs in water compared to oAs, iAs can accumulate more readily in tissues. When organisms are exposed to arsenic, the element is reduced and methylated to less- or non-toxic metabolites such as arsenocholine (AsC) and arsenobetaine (AsB) for excretion (Phillips, 1990; Kumaresan and Riyazuddin, 2001). This implies that arsenic biotransformation can be a major mechanism for detoxification.

Trophic transfer is another relevant issue, as arsenic can accumulate in higher-trophic-level organisms through the aquatic food web (Rahman et al., 2012). In the marine food web, biological accumulation of iAs can occur at three levels: autotrophs, grazers, and carnivores (Wrench et al., 1979). iAs can be produced through in vivo synthesis by primary producers and transferred efficiently through the marine food web. In addition, AsB concentration was reportedly found to increase with trophic level in marine organisms (Francesconi and Edmonds, 1996) such as the seabream Acanthopagrus schlegeli and the grunt Terapon jarbua (Zhang et al., 2016). In fact, the distribution and speciation of arsenic are largely attributed to the arsenic cycle in the aquatic environment, including biotransformation processes of aquatic organisms. Biological processes including trophic transfer are an important part of biogeochemical arsenic cycling in aquatic systems (Oremland and Stolz, 2003; Kalia and Khambholja, 2015).

Multiple studies have described the sources, chemistry, speciation, and toxicity of arsenic in aquatic ecosystems (Neff, 1997; Smedley and Kinniburgh, 2002; Akter et al., 2005; Pal et al., 2009; Kalia and Khambholja, 2015), but arsenic toxicity and bioavailability in aquatic organisms remain unclear. This review focuses on arsenic speciation and distribution in aquatic biota with an emphasis on the mechanisms of toxicity.