Toxicity mechanisms of arsenic compounds 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 (AsV), arsenite (AsIII), arsenic (As), and arsine (As−III) (Sharma and Sohn, 2009). Inorganic arsenic (iAs), AsV and AsIII, 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.
Section snippets
Arsenic chemistry and distribution in the aquatic environment
In natural environments, arsenic exists in four oxidation states (−3, 0, +3, and +5). The variable oxidation states of arsenic result in an extensive chemical reactivity due to high ability to bond with other elements, resulting in various forms of arsenic compounds. The chemical structures of environmentally important arsenic species are shown in Fig. 1. While the element itself does not dissolve well in water, arsenic compounds can be water soluble. Chemically, arsenic compounds appear in two
Oxidative stress-mediated mechanism
Oxidative stress is an inevitable aspect of aerobic environments and is caused by an imbalance between the production of reactive oxygen species (ROS) and antioxidant defense mechanisms in living organisms. ROS are highly reactive chemical molecules and is formed in biological systems during molecular oxygen reduction and include hydrogen peroxide (H2O2), hydroperoxyl radical (HOO•), hydroxyl radical (•OH), superoxide radical anion (O2−•), singlet oxygen (1O2), and peroxyl radical (ROO•) (
Marine organisms
The presence of arsenic in fish and marine organisms was first reported by Lunde (1977). In biological samples from marine environments, the average arsenic concentration of seawater is approximately 1.5 µg/L (Smedley and Kinniburgh, 2002). As mentioned in Section 2.1, arsenic concentrations in coastal waters are generally more variable than those of open seawater due to inflow of pollutants from land. If the concentration of environmental arsenic is high, arsenic is likely to accumulate to
Conclusions
Arsenic levels in freshwater environments are highly variable due to differences in sources, availability, and chemical properties of the environment. Although oceans generally have a lower arsenic level compared with freshwater ecosystems, estuarine and coastal waters can exhibit high arsenic levels due to inputs from land and other environmental factors. Exposure to arsenic and its bioaccumulation can cause various adverse effects in aquatic organisms.
The toxic effects of arsenic vary
Credit Author Statement
J.-S.L. and H.-M. K. designed and supervised the project. E.B., H.J., Y.L., U.-K.H., and C.-B.J. collected and generated the data, and C.Y. performed the analytical analyses. J.-S.L., C.-B.J., and H.-M. K. wrote the manuscript.
Declaration of Competing Interest
The authors declare no competing financial interest.
Acknowledgments
This work was supported by a grant from the National Research Foundation (2020R1F1A1076854) funded to Jae-Seong Lee.
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