Diverse arsenic‐containing lipids in the surface ocean

Abstract

Marine microbes experience constant exposure to the potentially toxic element arsenic. However, there are no baseline measurements of how much arsenic accumulates in microbial communities nor do we know the full spectrum of arsenic containing biomolecules produced in marine systems. In culture-based studies there is strong evidence that phytoplankton synthesize arsenic-containing lipids, but these lipids are only beginning to be explored within natural marine microbial communities. Here, we make measurements of bulk particulate arsenic at five sites in the surface open ocean and show that a significant portion of this particulate arsenic is present as complex arsenic-containing lipids. We characterize this arsenolipid pool chemically and quantitatively to show a variety of chemically distinct and quantitatively significant lipids that expand our understanding of marine arsenic biogeochemistry.Arsenic is present at nanomolar levels throughout the ocean, and microbes assimilate this potentially toxic element due to its similarity to inorganic phosphorus. Although dissolved arsenic has been a focus of several oceanographic studies, the size and chemical character of the particulate arsenic pool is poorly understood. We measured particulate arsenic in five samples from the open ocean and determined the contribution of arseniccontaining lipids to this pool. Here we show that the accumulation of arsenic into lipids is a widespread phenomenon in the surface ocean. Particulate arsenic concentrations were 15-42 pmol L À1 with 7-20% of the particulate arsenic pool within arsenolipids. We found that arsenosugar phospholipids dominated the arsenolipid pools in our samples with a minor component of arsenohydrocarbons and other unidentified lipids. A significant portion of the arsenosugar phospholipids (up to 35%) was present as previously undescribed mixed acyl ether lipids, suggesting a bacterial source.

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“…AsLs are neutral lipid analogs (Dembitsky & Levitsky, 2004) that are abundant in marine organisms (Al Amin et al, 2018, 2020; Amayo et al, 2013, 2014; Heal et al, 2022; Liu et al, 2022; Petursdottir et al, 2016; Taylor & Karagas, 2022; Tibon et al, 2022). AsL speciations primarily include arsenic‐containing hydrocarbons (AsHCs) (Arroyo‐Abad et al, 2010), arsenic‐containing fatty acids (Sele et al, 2014), and arsenic‐containing phospholipids (AsPLs) (Chen et al, 2023; Raab et al, 2013).…”

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“…Biogeochemical fluxes, and in some instances, their impacts on organismal physiology, was another theme of the selected studies. Heal et al (2022) shed new light on how marine microbial communities interact with and accumulate arsenic, a potentially toxic element. They showed that in the open ocean surface waters, much of the bulk particulate arsenic is actually contained in complex lipids, some of which appear to be of bacterial origin.…”