Arid
DOI10.1128/mBio.00246-19
A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton
Giovannoni, Stephen J.1; Halsey, Kimberly H.1; Saw, Jimmy1,2; Muslin, Omran1; Suffridge, Christopher P.1; Sun, Jing1,3; Lee, Chih-Ping1; Moore, Eric R.1; Temperton, Ben1,4; Noell, Stephen E.1
通讯作者Giovannoni, Stephen J.
来源期刊MBIO
ISSN2150-7511
出版年2019
卷号10期号:2
英文摘要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 [C-14]dimethyl arsenate (DMA) and used it to show that cultured Pelagibacter strain HTCC7211 (SAR11) cells oxidize the methyl group carbons of DMA, producing (CO2)-C-14 and ATP. We measured [C-14] DMA oxidation rates in the P-depleted surface waters of the Sargasso Sea, a subtropical ocean gyre. [C-14]DMA was oxidized to (CO2)-C-14 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.
英文关键词SAR11 arsenic ocean
类型Article
语种英语
国家USA ; Peoples R China ; England
开放获取类型Green Published, gold
收录类别SCI-E
WOS记录号WOS:000465077600037
WOS关键词OCEAN ; BIOGEOCHEMISTRY ; DEMETHYLATION ; LIMITATION ; TRANSPORT ; BACTERIA ; ANTIMONY ; ACID
WOS类目Microbiology
WOS研究方向Microbiology
资源类型期刊论文
条目标识符http://119.78.100.177/qdio/handle/2XILL650/217562
作者单位1.Oregon State Univ, Dept Microbiol, Corvallis, OR 97331 USA;
2.George Washington Univ, Washington, DC USA;
3.Chinese Acad Fishery Sci, Yellow Sea Fisheries Res Inst, Qingdao, Shandong, Peoples R China;
4.Univ Exeter, Biosci, Exeter, Devon, England
推荐引用方式
GB/T 7714
Giovannoni, Stephen J.,Halsey, Kimberly H.,Saw, Jimmy,et al. A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton[J],2019,10(2).
APA Giovannoni, Stephen J..,Halsey, Kimberly H..,Saw, Jimmy.,Muslin, Omran.,Suffridge, Christopher P..,...&Noell, Stephen E..(2019).A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton.MBIO,10(2).
MLA Giovannoni, Stephen J.,et al."A Parasitic Arsenic Cycle That Shuttles Energy from Phytoplankton to Heterotrophic Bacterioplankton".MBIO 10.2(2019).
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