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Research Article | Ecological and Evolutionary Science

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

Stephen J. Giovannoni, Kimberly H. Halsey, Jimmy Saw, Omran Muslin, Christopher P. Suffridge, Jing Sun, Chih-Ping Lee, Eric R. Moore, Ben Temperton, Stephen E. Noell
Jizhong Zhou, Editor
Stephen J. Giovannoni
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Kimberly H. Halsey
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Jimmy Saw
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Omran Muslin
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Christopher P. Suffridge
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Jing Sun
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Chih-Ping Lee
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Eric R. Moore
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Ben Temperton
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Stephen E. Noell
aDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Jizhong Zhou
University of Oklahoma
Roles: Editor
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John Stolz
Duquesne University
Roles: Solicited external reviewer
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Craig Nelson
University of Hawai‘i at Mānoa
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DOI: 10.1128/mBio.00246-19
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ABSTRACT

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 [14C]dimethyl arsenate (DMA) and used it to show that cultured Pelagibacter strain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing 14CO2 and ATP. We measured [14C]DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [14C]DMA was oxidized to 14CO2 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.

IMPORTANCE In vast, warm regions of the oceans, phytoplankton face the problem of arsenic poisoning. Arsenate is toxic because it is chemically similar to phosphate, a scarce nutrient that phytoplankton cells need for growth. Many phytoplankton, including the commonest phytoplankton type in warm oceans, Prochlorococcus, detoxify arsenate by adding methyl groups. Here we show that the most abundant non-photosynthetic plankton in the oceans, SAR11 bacteria, remove the methyl groups, releasing poisonous forms of arsenic back into the water. We postulate that the methylation and demethylation of arsenic compounds creates a cycle in which the phytoplankton can never get ahead and must continually transfer energy to the SAR11 bacteria. We dub this a parasitic process and suggest that it might help explain why SAR11 bacteria are so successful, surpassing all other plankton in their numbers. Field experiments were done in the Sargasso Sea, a subtropical ocean gyre that is sometimes called an ocean desert because, throughout much of the year, there is not enough phosphorous in the water to support large blooms of phytoplankton. Ocean deserts are expanding as the oceans absorb heat and grow warmer.

FOOTNOTES

    • Received 30 January 2019
    • Accepted 4 February 2019
    • Published 19 March 2019
  • Copyright © 2019 Giovannoni et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
Stephen J. Giovannoni, Kimberly H. Halsey, Jimmy Saw, Omran Muslin, Christopher P. Suffridge, Jing Sun, Chih-Ping Lee, Eric R. Moore, Ben Temperton, Stephen E. Noell
mBio Mar 2019, 10 (2) e00246-19; DOI: 10.1128/mBio.00246-19

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A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
Stephen J. Giovannoni, Kimberly H. Halsey, Jimmy Saw, Omran Muslin, Christopher P. Suffridge, Jing Sun, Chih-Ping Lee, Eric R. Moore, Ben Temperton, Stephen E. Noell
mBio Mar 2019, 10 (2) e00246-19; DOI: 10.1128/mBio.00246-19
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KEYWORDS

SAR11
arsenic
ocean

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