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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...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2019
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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. |
format | Online Article Text |
id | pubmed-6426599 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
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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