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

Abstract

Studies of cyanobacteria in environments where arsenic (As) and phosphate (P) both occur in significant concentrations have so far only focused on the effect of P on As(V) toxicity and bioaccumulation, with little attention to the influence of P on As redox transformations. Our study revealed that As(III) oxidation by Synechocystis appeared to be more effective with increased P levels. We demonstrated that the higher As(III) percentage in the medium under P-limited conditions was due to enhanced As(V) uptake and the subsequent efflux of intracellularly reduced As(III) which in turn contributed to higher As(III) concentrations in the medium. Arsenic redox changes by Synechocystis under P-limited conditions is a dynamic cyclic process that includes the following: surface As(III) oxidation (either in the periplasm or near the outer membrane), As(V) uptake, intracellular As(V) reduction, and As(III) efflux. These observations not only expand our understanding of how P influences microbial As redox metabolisms but also provide insights into the biogeochemical coupling between As and P in As contaminated eutrophic aquatic environments and artificial wetland-paddy fields. ■ INTRODUCTIONArsenic (As) is a ubiquitous toxic substance broadly distributed in the environment. 1 The transport and transformation of As in environment are governed by geochemical and biological processes, generating an As biogeochemical cycle. 2 Microbially mediated biotransformations may play an important role in determining As biogeochemistry and toxicity in various natural ecosystems, especially As redox processes which influence the two most abundant inorganic As forms (arsenite As(III) and arsenate As(V)) in the environment. 3 Thus it is essential to understand microbial As redox metabolisms to make further advances in As bioremediation.Microalgae are desirable organisms for As remediation in contaminated water because of their high surface area to volume ratios. 4 Studies have shown that microalgae can tolerate high levels of As and biotransform it in several ways to detoxify it. 5−9 Considering the complex living environments of microalgae, many factors could affect As biotransformations by microalgae. Phosphate (P) is one of the most significant determinants of microalgal growth. 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. 13,14 In the bacteria Agrobacterium tumefaciens str. 5B, it has been reported that As(V) reduction was completely suppressed at elevated levels of P (500 and 1000 μM), but the expression of the As(V) reductase gene (arsC) was not inhibited by high P concentrations. 15 As(III) oxidation and the Phosphorus (Pi) concentration were reported to be tightly and intimately coregulated in the soil bacterium Agrobacterium tumefaciens. 16 However, when analyzing ...

Review of arsenic speciation, toxicity and metabolism in microalgae

“…PO 4 -riboside) were produced by D. tertiolecta under P-limited conditions. Zhang et al (2014) demonstrated that As(III) oxidation by Synechocystis appeared to be more effective with increased PO 4 3-concentrations. Accordingly, future research should focus on the intracellular ratio of As/P and its effect on As(V) accumulation and speciation in microalgae.…”

“…There are many abiotic factors affecting the As metabolism of microalgae, such as the composition of growth medium (Hasegawa et al 2001;Wurl et al 2013), arsenic species and levels (Gong et al 2009;Hasegawa et al 2001;Karadjova et al 2008;Maeda et al 1985;Yamaoka et al 1996), hydrogen ion concentration (pH) (Hasegawa et al 2001;Maeda et al 1992;Murray et al 2003;Pawlik-Skowrońska et al 2004;Taboada-de la Calzada et al 1999;Zhang et al 2013a), temperature (Maeda et al 1985;Taboada-de la Calzada et al 1999), redox potential (Eh) (Murray et al 2003;Wang et al 2013a), exposure duration (Foster et al 2008;Zhang et al 2014), light intensity (Bottino et al 1978;Budd and Craig 1981;Karadjova et al 2008;Maeda et al 1985;PawlikSkowrońska et al 2004;Taboada-de la Calzada et al 1999;Yamaoka et al 1999), etc. For example, using the same growth medium (f/2 medium), Duncan et al (2010) found the total As accumulated by Dunaliella tertiolecta was 2.2-fold lower than that found by Foster et al (2008), in which the same microalgae were incubated in the same As(V) exposure concentration (2 lg/L).…”

“…), As(V) is absorbed into cells via phosphate transporters, while As(III) moves across plasma membrane via aquaglyceroporins (AQP) and hexose permeases (Cullen et al 1994;Levy et al 2005;Zhang et al 2014). The chemical similarity between PO 4 3-and AsO 4 3-suggests that these ions may show competitive behavior with regard to the phosphate uptake system (Andreae and Klumpp 1979;Johnson 1971;Xue et al 2014).…”

“…Long-term exposure of As at low doses can lead to chronic arsenic poisoning and increase risks of skin, lung and bladder cancers (Saha et al 1999). Owing to this fact, studies on distribution and behavior of As in the environment, metabolism and resistance mechanisms of As in microorganisms and bioremediation of the As-polluted environment have gained considerable attention (Foster et al 2008;Karadjova et al 2008;Mertens 2011;Velizarov et al 2004;Yamaoka et al 1999;Yin et al 2012;Zhang et al 2014).…”

The mechanisms of detoxification of As(III), dimethylarsinic acid (DMA) and As(V) in the microalga Chlorella vulgaris

“…After exposure to As(III), only trace amounts of As(V) and DMA were observed inside the algae, by contrast, other researchers have reported up to 67% oxidation inside microalgae (Wang et al, 2014) and 45% oxidation in cyanobacteria, although the later was measured in growing media (Zhang et al, 2014).…”