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

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-m...

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Autores principales: Glabonjat, Ronald A., Blum, Jodi S., Miller, Laurence G., Webb, Samuel M., Stolz, John F., Francesconi, Kevin A., Oremland, Ronald S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7345539/
https://www.ncbi.nlm.nih.gov/pubmed/32599768
http://dx.doi.org/10.3390/life10060093
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author Glabonjat, Ronald A.
Blum, Jodi S.
Miller, Laurence G.
Webb, Samuel M.
Stolz, John F.
Francesconi, Kevin A.
Oremland, Ronald S.
author_facet Glabonjat, Ronald A.
Blum, Jodi S.
Miller, Laurence G.
Webb, Samuel M.
Stolz, John F.
Francesconi, Kevin A.
Oremland, Ronald S.
author_sort Glabonjat, Ronald A.
collection PubMed
description 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.
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spelling pubmed-73455392020-07-09 Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California Glabonjat, Ronald A. Blum, Jodi S. Miller, Laurence G. Webb, Samuel M. Stolz, John F. Francesconi, Kevin A. Oremland, Ronald S. Life (Basel) Article 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. MDPI 2020-06-24 /pmc/articles/PMC7345539/ /pubmed/32599768 http://dx.doi.org/10.3390/life10060093 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Glabonjat, Ronald A.
Blum, Jodi S.
Miller, Laurence G.
Webb, Samuel M.
Stolz, John F.
Francesconi, Kevin A.
Oremland, Ronald S.
Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title_full Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title_fullStr Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title_full_unstemmed Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title_short Arsenolipids in Cultured Picocystis Strain ML and Their Occurrence in Biota and Sediment from Mono Lake, California
title_sort arsenolipids in cultured picocystis strain ml and their occurrence in biota and sediment from mono lake, california
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7345539/
https://www.ncbi.nlm.nih.gov/pubmed/32599768
http://dx.doi.org/10.3390/life10060093
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