Biosynthesis of arsenolipids by the cyanobacterium Synechocystis sp. PCC 6803

Abstract

Environmental context. Arsenic biotransformation processes play a key role in the cycling of arsenic in aquatic systems. We show that a freshwater cyanobacterium can convert inorganic arsenic into arsenolipids, and the conversion efficiency depends on the arsenic concentration. The role of these novel arsenic compounds remains to be elucidated.Abstract. Although methylated arsenic and arsenosugars have been verified in various freshwater organisms, lipidsoluble arsenic compounds have not been identified. Here, we report investigations with the model organism cyanobacterium Synechocystis sp. PCC 6803 wild type and DarsM (arsenic(III) S-adenosylmethionine methyltransferase) mutant strain, which lacks the enzymes for arsenic methylation cultured in various concentrations of arsenate (As V ). Although Synechocystis accumulated higher arsenic concentrations at the higher exposure levels, the bioaccumulation factor decreased with increasing As V . The accumulated arsenic in the cells was partitioned into water-soluble and lipidsoluble fractions; lipid-soluble arsenic was found in Synechocystis wild type cells (3-35 % of the total depending on the level of arsenic exposure), but was not detected in Synechocystis DarsM mutant strain showing that ArsM was required for arsenolipid biosynthesis. The arsenolipids present in Synechocystis sp. PCC 6803 were analysed by high performance liquid chromatography-inductively coupled plasma-mass spectrometry, high performance liquid chromatographyelectrospray mass spectrometry, and high resolution tandem mass spectrometry. The two major arsenolipids were characterised as arsenosugar phospholipids based on their assigned molecular formulas C 47 H 88 O 14 AsP and C 47 H 90 O 14 AsP, and tandem mass spectrometric data demonstrated the presence of the phosphate arsenosugar and acylated glycerol groups.Additional keyword: arsenic.

Review of arsenic speciation, toxicity and metabolism in microalgae

“…In the past few years, the investigation of As-containing lipids (arsenolipids) and their possible role in the transformation and detoxification of As have gained interest. However, the structures of arsenolipids and derivatives in microalgae have been consistently overlooked while some of them have been identified (Dembitsky and Levitsky 2004;García-Salgado et al 2012b;Xue et al 2014). Moreover, identity and toxicity of these compounds are largely unknown due to lower levels of the lipid-soluble arsenic species in the marine environment, as well as difficulties associated with isolation and analysis of these compounds compared to water-soluble arsenic species (Dembitsky and Levitsky 2004;Duncan et al 2013aDuncan et al , b, 2015.…”

“…), 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).…”

“…Moreover, identity and toxicity of these compounds are largely unknown due to lower levels of the lipid-soluble arsenic species in the marine environment, as well as difficulties associated with isolation and analysis of these compounds compared to water-soluble arsenic species (Dembitsky and Levitsky 2004;Duncan et al 2013aDuncan et al , b, 2015. The synthesis of lipid-soluble As compounds has been demonstrated in green algae C. vulgaris, Chlorella ovalis, Chlorella pyrenoidosa and D. tertiolecta, bluegreen algae Oscillatoria rubescence and Synechocystis and diatoms Phaeodactylum tricornutum, S. costatum and T. pseudonana (Duncan et al 2013a(Duncan et al , b, 2014Foster et al 2008;Lunde 1973;Murray et al 2003;Wrench and Addison 1981;Xue et al 2014). Wrench and Addison (1981) reported the presence of three arsenolipids in the unicellular marine phytoplankton, D. tertiolecta.…”

“…This is further supported by the study of Foster et al (2008) who showed that D. tertiolecta and P. tricornutum contained 29-38 % and 20-29 % of the total As as lipid-soluble As, respectively. Recently, Xue et al (2014) showed that, upon As(V) exposure, a freshwater microalga Synechocystis sp. PCC 6803 could produce arsenosugar phospholipid (a class of arsenolipids) and this was dependent on the catalysis by As(III) methyltransferase (ArsM).…”

Periphyton and abiotic factors influencing arsenic speciation in aquatic environments

“…Laboratory studies have shown that a variety of aquatic microalgae and bacteria species are capable of oxidizing As(III) to As(V) [35][36][37], reducing As(V) to As(III) [38,39], biomethylating As [38,40], or synthesizing complex arsenosugars or arsenolipids [35,41,42]. Laboratory studies have shown that a variety of aquatic microalgae and bacteria species are capable of oxidizing As(III) to As(V) [35][36][37], reducing As(V) to As(III) [38,39], biomethylating As [38,40], or synthesizing complex arsenosugars or arsenolipids [35,41,42].…”