Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California

Abstract

Primary production in Mono Lake, a hypersaline soda lake rich in dissolved inorganic arsenic, is dominated by Picocystis strain ML. We set out to determine if this photoautotrophic picoplankter could metabolize inorganic arsenic and in doing so form unusual arsenolipids (e.g., arsenic bound to 2-O-methyl ribosides) as reported in other saline ecosystems and by halophilic algae. We cultivated Picocystis strain ML on a seawater-based medium with either low (37 µM) or high (1000 µM) phosphate in the presence of arsenite (400 µM), arsenate (800 µM), or without arsenic additions (ca 0.025 µM). Cultivars formed a variety of organoarsenic compounds, including a phytyl 2-O-methyl arsenosugar, depending upon the cultivation conditions and arsenic exposure. When the cells were grown at low P, the organoarsenicals they produced when exposed to both arsenite and arsenate were primarily arsenolipids (~88%) with only a modest content of water-soluble organoarsenic compounds (e.g., arsenosugars). When grown at high P, sequestration shifted to primarily water-soluble, simple methylated arsenicals such as dimethylarsinate; arsenolipids still constituted ~32% of organoarsenic incorporated into cells exposed to arsenate but < 1% when exposed to arsenite. Curiously, Picocystis strain ML grown at low P and exposed to arsenate sequestered huge amounts of arsenic into the cells accounting for 13.3% of the dry biomass; cells grown at low P and arsenite exposure sequestered much lower amounts, equivalent to 0.35% of dry biomass. Extraction of a resistant phase with trifluoroacetate recovered most of the sequestered arsenic in the form of arsenate. Uptake of arsenate into low P-cultivated cells was confirmed by X-ray fluorescence, while XANES/EXAFS spectra indicated the sequestered arsenic was retained as an inorganic iron precipitate, similar to scorodite, rather than as an As-containing macromolecule. Samples from Mono Lake demonstrated the presence of a wide variety of organoarsenic compounds, including arsenosugar phospholipids, most prevalent in zooplankton (Artemia) and phytoplankton samples, with much lower amounts detected in the bottom sediments. These observations suggest a trophic transfer of organoarsenicals from the phytoplankton (Picocystis) to the zooplankton (Artemia) community, with efficient bacterial mineralization of any lysis-released organoarsenicals back to inorganic oxyanions before they sink to the sediments.

Diverse arsenic-containing lipids in the surface ocean

“…Lund 1973;Amayo et al 2013;Raab et al 2013;Taleshi et al 2014;Xue et al 2014;Glabonjat et al 2018). Algal and cyanobacterial monocultures vary widely in the percent of total cellular arsenic present as arsenolipids in large part because of accumulated or sorbed inorganic arsenic (Duncan et al 2013;Xue et al 2014;Glabonjat et al 2018Glabonjat et al , 2020. Our observations of 7-20% of total particulate arsenic as arsenolipids is on the higher end of these observations.…”

“…Most of the literature suggest eukaryotic algae as the main source of arsenolipids in natural systems (Glabonjat et al 2019(Glabonjat et al , 2020. Our provocative findings of AsSugPeL lipids suggest at least some of the lipids may be of bacterial origin.…”

“…Our measurements show that particulate arsenic is nearly 1000 times less abundant than dissolved arsenic. This high seawater background obscures our view of transformations of arsenic occurring within or on particles and has hindered measurements of suspended particulate arsenic in aquatic systems for decades (Andreae 1978; Glabonjat et al 2020). This background is important to take into consideration when loading particulate material onto a filter for analysis — we filtered 193–747 L of surface seawater onto 142 mm filter (Table S2).…”

“…No other marine observations of arsenolipids have been made, but recent work has characterized arsenolipids in sediments and suspended matter in relatively arsenic-rich lakes like Mono Lake in California (Glabonjat et al 2020) and the Great Salt Lake in Utah (Glabonjat et al 2019). At both locations, arsenolipid composition was dominated by a rich array of isoprenoidal arsenolipids related to phytol, hypothesized to be produced by green algae including Picocystis which dominate the Mono Lake phytoplankton community (Glabonjat et al 2020). Additional green algae species produce arsenolipids of similar structure (Glabonjat et al 2018; Řezanka et al 2019).…”

“…Taleshi et al 2014) and are produced by monocultures of green algae, diatoms, and cyanobacteria in laboratory settings (Duncan et al 2013;Xue et al 2014;Řezanka et al 2019). Arsenolipids have also been observed in lake sediments and lacustrine suspended particles (Glabonjat et al 2019(Glabonjat et al , 2020. Together, these findings suggest that the production of organic arsenic compounds is a widespread process in aquatic settings.…”