Arsenosugars and arsenolipids are formed simultaneously by the unicellular alga Dunaliella tertiolecta

Abstract

Environmental context: Arsenic is a globally distributed element, occurring in various chemical forms with toxicities ranging from harmless to highly toxic. We conducted 48-h cell culture experiments under batch and continuous conditions using the ubiquitous marine unicellular alga Dunaliella tertiolecta and evaluated the alga's arsenic metabolome over time. We found that the alga first methylates the inorganic As taken up from the surrounding water, and then further metabolises the intermediate simultaneously into more complex organo-arsenic molecules like sugars and lipids. These time series experiments are valuable pieces in the puzzle of how algae bio-metabolise arsenic, and in our understanding of the global arsenic cycle. Rationale: The uptake of arsenate by algae from oceanic waters and its transformation to arsenosugars and arsenolipids is well established, but the biosynthetic pathways remain largely unknown. Methodology: We investigated these pathways by using time-series experiments over 48 h to follow the formation of organoarsenic species from arsenate-enriched medium (15 µg As L-1) by the unicellular alga Dunaliella tertiolecta cultured under batch and continuous culture conditions. We used complementary mass spectrometry methods for the determination and quantification of 14 arsenic species; an additional three species could be quantified but remained unidentified. Results: The alga rapidly methylated the arsenate to dimethylarsinate (DMA), which then served as the precursor to arsenosugars and arsenolipids; the concentrations of these complex organoarsenicals increased throughout the experiments accompanied by a concomitant reduction in DMA concentrations. The pattern of compounds formed by the alga was similar for both batch and continuous cultures, but the concentrations were 2-3-fold higher in the continuous culture samples and the increases with time were much clearer. Discussion: The data suggest that the arsenosugars and the arsenolipids were mostly formed simultaneously from DMA, although there was an indication that the arsenic phospholipids were at least partly also being formed from the arsenosugars. Overall, the data are consistent with a direct biosynthesis of DMA from arsenate by D. tertioleta, and thereafter a non-specific incorporation of DMA into commonly available alga metabolites encompassing various sugars and lipids. Show more