Chemical and genetic evidence point to arseno-metabolites underpinning the marine arsenic cycle

Arsenic has a bad reputation. It’s probably best known for killing Napoleon Bonaparte and for being front and center during a geobiology publication nightmare a decade ago. Arsenic’s well known toxicity arises from its structural similarity to phosphorus and the ‘accidental’ substitution of As in place of P due to enzyme promiscuity. In areas with low P like the oligotrophic surface ocean, concentrations of dissolved As can rival P, driving the microbial community to use a myriad of techniques to differentiate the two elements in order to process P appropriately. We propose that phytoplankton in environments with high As:P reduce As and synthesize metabolites like arseno-sugars and arseno-lipids. We support this hypothesis through mining transcriptomes for As-related genes, making geochemical measurements for As in different fractions of particles, and searching for arseno-organic compounds in metabolomics datasets. Transcriptomes suggest that picocyanobacteria are at the heart of the first step in the biosynthesis of areseno-organic compounds in low P environments. Our particulate arsenic measurements show that particulate As is found mostly bound in water-soluble compounds, but up to 15% can be found in lipid-like compounds, supporting the presence of arseno-lipids in the open ocean. Finally, our metabolomic data suggest that these areseno-metabolites are reworked throughout the water column into arsenobetaine (an analog to the common osmolyte glycine betaine in which N is replaced with As), before the arsenic is fully oxididized back to arsenate to complete the arsenic cycle. The synthesis of arseno-metabolites allows cells to differentiate the elements and possibly use As for a biological purpose, which is especially important for marine organisms that consistently encounter low macronutrients.