Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae

Abstract

Environmental context. Although organoarsenic compounds occur in marine organisms at high concentrations, the origin and role of these compounds is unknown. Arsenic-containing lipids (arsenolipids) are newly discovered compounds in fish. We identify a range of arsenolipids in algae and propose that algae are the origin of these unusual arsenic compounds in marine ecosystems.Abstract. Fourteen arsenolipids, including 11 new compounds, were identified and quantified in two species of brown algae, Wakame (Undaria pinnatifida) and Hijiki (Hizikia fusiformis), by high resolution mass spectrometry, high performance liquid chromatography-mass spectrometry and gas chromatography-mass spectrometry. Both algal species contained arsenosugar-phospholipids as the major type of arsenolipid, and arsenic-hydrocarbons were also significant components, particularly in Hijiki. The origin of the various arsenolipids, and the possible significance of their relative quantities, is briefly discussed. Arsenic-containing organic compounds are abundant in marine ecosystems where they are thought to play a pivotal role in the cycling and detoxification of potentially toxic inorganic arsenic (arsenate) present in seawater. [1] Although most of the arsenic compounds identified so far have been water-soluble species, the early work on arsenic marine chemistry focussed on lipidsoluble compounds, so called arsenolipids. [2][3][4] Identification of these arsenolipids proved difficult, however, and it was not until 1988 that an arsenolipid was first rigorously characterised and identified as an arsenosugar-containing phospholipid [5] (see Table 1, compound As-PL958).Subsequently, the range of naturally occurring arsenolipids has been extended with the discovery of arsenic-containing fatty acids in fish oils, [6] and arsenic-containing hydrocarbons in fish oils, [7] fish liver, [8] sashimi tuna [9] and fish meal. [10] The origin of these compounds was presumed to be algae. We report the arsenolipid profiles of two species of brown algae, determined mainly by high performance liquid chromatography-mass spectrometry (HPLC-MS), and we briefly discuss the possible biosynthetic origin of these unusual compounds.Samples of Wakame (Undaria pinnatifida, 40 AE 3 mg As g À1 dry mass) and Hijiki (Hizikia fusiformis, 113 AE 5 mg As g À1 dry mass), A obtained from a Japanese commercial source, were extracted with a mixture of chloroform and methanol using a modification B of the classical procedure of Bligh and Dyer. [11] The lipid fraction containing 6.7 % (Wakame) and 1.6 % (Hijiki)A Determination of arsenic contents. Total arsenic analyses were performed on portions of the dry powders, extracts or combined fractions from the silica columns by ICP-MS (Agilent 7500ce) in helium collision cell mode following a microwave-assisted acid mineralisation step. The method was validated by analysis of reference material NIES No. 9 Sargasso (certified As content 115 AE 5 mg As g À1 ); we obtained 116 AE 2 mg As g À1 (n ¼ 3). BExtraction and purification of arsenolipid...

Cyanobacteria produce arsenosugars

“…production of lipid-soluble As compounds for membrane lipid bilayers). Many marine algae have arsenolipids including phosphatidyldimethylarsinylribose (usually termed phosphatidylarsenosugar, an arsenoribosyl derivative of phosphatidyl glycerol and a derivative of Oxo-PO 4 ), [43][44][45] and the arsenolipids are speculated to be included in the lipid bilayer structures of the algal outer membrane. [44] If cyanobacteria produce similar arsenolipids, they may be located at the cell membrane or thylakoid membrane, as well as phosphatidyl glycerol.…”

Environmental effects on arsenosugars and arsenolipids in Ectocarpus (Phaeophyta)

“…[12] Four AsHCs were identified here (Table 2); the main AsHC360 is commonly found both in fish and algae, whereas AsHC374 and AsHC388 (found in field-collected Ectocarpus and cultures) have only been identified before in algae. [11,12] The ten AsPLs identified here have been reported in previous studies (Table 2). 57 % AE 9 (n ¼ 3) for Elachista, 75 % AE 5 (n ¼ 6) for Ectocarpus from Reykjavík and 76 % AE 7 (n ¼ 6) for Ectocarpus from Aberdeen, Table 2 (detailed quantification for each species is given in Supplementary Tables S8-S12).…”

“…by using AsPLs to replace phospholipids. [11,13] Benson and coworkers [14] grew algal cultures in 74 As V and showed that the arsenate was taken up by the algae, where the first biotransformation intermediates were lipid-soluble As species, thought to be AsPL. The AsPLs might therefore be formed first where the arsenosugars (AsSugars) are subsequently a hydrolysed product of the AsPLs.…”

“…Most arsenosugars are dimethylarsinoylribosides and most can be associated with just four compounds, although 20 naturally occurring arsenosugars have been identified. [4] Recently, it was established that besides arsenosugars, arsenic can form lipid-soluble dimethylarsinoyl species in seaweeds, [11,12] i.e. hydrocarbons (AsHC), fatty acids (AsFA) and phospholipids (AsPL), Fig.…”

Recent advances in speciation analysis of mercury, arsenic and selenium

“…Recently, 14 arsenolipids, including 11 new compounds, were identified and quantified in brown algae, wakame (Undaria pinnatifida) and hijiki (Hizikia fusiformis), by HPLC-MS and GC-MS [19]. Both algal species contained arsenosugarphospholipids as the major type of arsenolipid, and arsenic-hydrocarbons were also detected, especially in Hijiki, suggesting that algae are the possible origin of these arsenolipids in marine ecosystems.…”