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

Katherine Heal1, Angela Boysen2, Bryndan Paige Durham3, Laura Carlson3, E. Virginia Armbrust2, Anitra E Ingalls4 and Randelle M Bundy4, (1)Pacific Northwest National Laboratories, United States, (2)University of Washington, School of Oceanography, Seattle, United States, (3)University of Washington, School of Oceanography, Seattle, WA, United States, (4)University of Washington Seattle Campus, School of Oceanography, Seattle, United States
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.