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A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton

In many regions of the world oceans, phytoplankton face the problem of discriminating between phosphate, an essential nutrient, and arsenate, a toxic analogue. Many phytoplankton, including the most abundant phytoplankton group known, Prochlorococcus, detoxify arsenate (AsV) by reduction to arsenite...

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Autores principales: Giovannoni, Stephen J., Halsey, Kimberly H., Saw, Jimmy, Muslin, Omran, Suffridge, Christopher P., Sun, Jing, Lee, Chih-Ping, Moore, Eric R., Temperton, Ben, Noell, Stephen E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426599/
https://www.ncbi.nlm.nih.gov/pubmed/30890605
http://dx.doi.org/10.1128/mBio.00246-19
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author Giovannoni, Stephen J.
Halsey, Kimberly H.
Saw, Jimmy
Muslin, Omran
Suffridge, Christopher P.
Sun, Jing
Lee, Chih-Ping
Moore, Eric R.
Temperton, Ben
Noell, Stephen E.
author_facet Giovannoni, Stephen J.
Halsey, Kimberly H.
Saw, Jimmy
Muslin, Omran
Suffridge, Christopher P.
Sun, Jing
Lee, Chih-Ping
Moore, Eric R.
Temperton, Ben
Noell, Stephen E.
author_sort Giovannoni, Stephen J.
collection PubMed
description In many regions of the world oceans, phytoplankton face the problem of discriminating between phosphate, an essential nutrient, and arsenate, a toxic analogue. Many phytoplankton, including the most abundant phytoplankton group known, Prochlorococcus, detoxify arsenate (AsV) by reduction to arsenite (AsIII), followed by methylation and excretion of the methylated arsenic products. We synthesized [(14)C]dimethyl arsenate (DMA) and used it to show that cultured Pelagibacter strain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing (14)CO(2) and ATP. We measured [(14)C]DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [(14)C]DMA was oxidized to (14)CO(2) by Sargasso Sea plankton communities at a rate that would cause turnover of the estimated DMA standing stock every 8.1 days. SAR11 strain HTCC7211, which was isolated from the Sargasso Sea, has a pair of arsenate resistance genes and was resistant to arsenate, showing no growth inhibition at As/P ratios of >65:1. Across the global oceans, there was a strong inverse relationship between the frequency of the arsenate reductase (LMWPc_ArsC) in Pelagibacter genomes and phosphate concentrations. We propose that the demethylation of methylated arsenic compounds by Pelagibacter and possibly other bacterioplankton, coupled with arsenate resistance, results in the transfer of energy from phytoplankton to bacteria. We dub this a parasitic cycle because the release of arsenate by Pelagibacter in principle creates a positive-feedback loop that forces phytoplankton to continually regenerate arsenate detoxification products, producing a flow of energy to P-limited ocean regions.
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spelling pubmed-64265992019-03-22 A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton Giovannoni, Stephen J. Halsey, Kimberly H. Saw, Jimmy Muslin, Omran Suffridge, Christopher P. Sun, Jing Lee, Chih-Ping Moore, Eric R. Temperton, Ben Noell, Stephen E. mBio Research Article In many regions of the world oceans, phytoplankton face the problem of discriminating between phosphate, an essential nutrient, and arsenate, a toxic analogue. Many phytoplankton, including the most abundant phytoplankton group known, Prochlorococcus, detoxify arsenate (AsV) by reduction to arsenite (AsIII), followed by methylation and excretion of the methylated arsenic products. We synthesized [(14)C]dimethyl arsenate (DMA) and used it to show that cultured Pelagibacter strain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing (14)CO(2) and ATP. We measured [(14)C]DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [(14)C]DMA was oxidized to (14)CO(2) by Sargasso Sea plankton communities at a rate that would cause turnover of the estimated DMA standing stock every 8.1 days. SAR11 strain HTCC7211, which was isolated from the Sargasso Sea, has a pair of arsenate resistance genes and was resistant to arsenate, showing no growth inhibition at As/P ratios of >65:1. Across the global oceans, there was a strong inverse relationship between the frequency of the arsenate reductase (LMWPc_ArsC) in Pelagibacter genomes and phosphate concentrations. We propose that the demethylation of methylated arsenic compounds by Pelagibacter and possibly other bacterioplankton, coupled with arsenate resistance, results in the transfer of energy from phytoplankton to bacteria. We dub this a parasitic cycle because the release of arsenate by Pelagibacter in principle creates a positive-feedback loop that forces phytoplankton to continually regenerate arsenate detoxification products, producing a flow of energy to P-limited ocean regions. American Society for Microbiology 2019-03-19 /pmc/articles/PMC6426599/ /pubmed/30890605 http://dx.doi.org/10.1128/mBio.00246-19 Text en Copyright © 2019 Giovannoni et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Giovannoni, Stephen J.
Halsey, Kimberly H.
Saw, Jimmy
Muslin, Omran
Suffridge, Christopher P.
Sun, Jing
Lee, Chih-Ping
Moore, Eric R.
Temperton, Ben
Noell, Stephen E.
A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title_full A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title_fullStr A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title_full_unstemmed A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title_short A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
title_sort parasitic arsenic cycle that shuttles energy from phytoplankton to heterotrophic bacterioplankton
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6426599/
https://www.ncbi.nlm.nih.gov/pubmed/30890605
http://dx.doi.org/10.1128/mBio.00246-19
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