Toxicity, biotransformation, and mode of action of arsenic in two freshwater microalgae (Chlorella sp. and Monoraphidium arcuatum)

Abstract

The toxicity of As(V) and As(III) to two axenic tropical freshwater microalgae, Chlorella sp. and Monoraphidium arcuatum, was determined using 72-h growth rate-inhibition bioassays. Both organisms were tolerant to As(III) (72-h concentration to cause 50% inhibition of growth rate [IC50], of 25 and 15 mg As[III]/L, respectively). Chlorella sp. also was tolerant to As(V) with no effect on growth rate over 72 h at concentrations up to 0.8 mg/L (72-h IC50 of 25 mg As[V]/L). Monoraphidium arcuatum was more sensitive to As(V) (72-h IC50 of 0.25 mg As[V]/L). An increase in phosphate in the growth medium (0.15-1.5 mg PO4(3-)/L) decreased toxicity, i.e., the 72-h IC50 value for M. arcuatum increased from 0.25 mg As(V)/L to 4.5 mg As(V)/L, while extracellular As and intracellular As decreased, indicating competition between arsenate and phosphate for cellular uptake. Both microalgae reduced As(V) to As(III) in the cell, with further biological transformation to methylated species (monomethyl arsonic acid and dimethyl arsinic acid) and phosphate arsenoriboside. Less than 0.01% of added As(V) was incorporated into algal cells, suggesting that bioaccumulation and subsequent methylation was not the primary mode of detoxification. When exposed to As(V), both species reduced As(V) to As(III); however, only M. arcuatum excreted As(III) into solution. Intracellular arsenic reduction may be coupled to thiol oxidation in both species. Arsenic toxicity most likely was due to arsenite accumulation in the cell, when the ability to excrete and/or methylate arsenite was overwhelmed at high arsenic concentrations. Arsenite may bind to intracellular thiols, such as glutathione, potentially disrupting the ratio of reduced to oxidized glutathione and, consequently, inhibiting cell division.

Arsenic speciation and effect of arsenate inhibition in a Microcystis aeruginosa culture medium under different phosphate regimes

“…The studies showed that less than 0.01% of arsenate added could be incorporated into algal cells [2]. The growth of M. aeruginosa was markedly inhibited by arsenate, and the inhibition was greater at high arsenate concentration than at low concentration (Fig.…”

“…1). The toxicity of intracellular arsenite, derived from arsenate in medium, was speculated to be one reason for the inhibition of arsenate [2]. Moreover, arsenate could induce the accumulation of reactive oxygen species (ROS) in the cells of cyanobacteria [25], and overaccumulation of ROS could result in cell death [26].…”

“…Arsenic exists commonly in freshwater as arsenate, arsenite, monomethylarsenicals (MMA), and dimethylarsenicals (DMA). The biotoxicity of As is dependent on its speciation, and the rank order of arsenical toxicity is as follows: MMA (III) -> arsenite > arsenate > DMA (V) [2,3]. Under aerobic conditions, pentavalent As is more stable and predominant, whereas trivalent species predominate under anaerobic conditions [4].…”

“…As an analogue of phosphate structure [16,17], arsenate can be absorbed by Microcystis along with the uptake patterns of phosphate when arsenate and phosphate coexist, and arsenate uptake affected microcystin content in the medium [18]. Levy et al [2] reported that the increase in phosphate decreased uptake of arsenate by freshwater microalgae and that a competition between arsenate and phosphate for cellular uptake existed. However, the uptake model proposed by Hellweger [10] accounted for a synergistic effect of high phosphate concentrations on arsenate uptake, which emerged in the former experiments [19].…”

Cyanobacteria-Mediated Arsenic Redox Dynamics Is Regulated by Phosphate in Aquatic Environments

“…Due to its structural similarity with As(V), 10 the influence of P on microbial As metabolisms has been extensively studied and primarily focused on As(V) accumulation and toxicity. 11,12 Besides affecting As(V) uptake, P can further influence the subsequent As detoxification process, i.e. As(V) reduction.…”