Synthesis of Methylphosphonic Acid by Marine Microbes: A Source for Methane in the Aerobic Ocean

Institute for Genomic Biology, University of Illinois, Urbana, IL 61801, USA.
Science (Impact Factor: 33.61). 08/2012; 337(6098):1104-7. DOI: 10.1126/science.1219875
Source: PubMed


Relative to the atmosphere, much of the aerobic ocean is supersaturated with methane; however, the source of this important greenhouse gas remains enigmatic. Catabolism of methylphosphonic acid by phosphorus-starved marine microbes, with concomitant release of methane, has been suggested to explain this phenomenon, yet methylphosphonate is not a known natural product, nor has it been detected in natural systems. Further, its synthesis from known natural products would require unknown biochemistry. Here we show that the marine archaeon Nitrosopumilus maritimus encodes a pathway for methylphosphonate biosynthesis and that it produces cell-associated methylphosphonate esters. The abundance of a key gene in this pathway in metagenomic data sets suggests that methylphosphonate biosynthesis is relatively common in marine microbes, providing a plausible explanation for the methane paradox.

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Available from: Sarath Chandra Janga, Mar 06, 2014
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    • "However, the problems of this approach at least include: 1) there are no " universal primers " for all taxa (including bacteria, archaea, fungi and virus) and therefore optimized PCR can only obtain part of the biodiversity information; and 2) PCR amplification efficiency may be biased toward a limited number of taxa. Since 2005, high-throughput sequencing (HTS) technologies have been applied as novel promising methods to investigate biodiversity and metabolic function of various communities, including human guts (Karlsson et al., 2013; Qin et al., 2010; Ridaura et al., 2013; Schloissnig et al., 2013), oral cavity (Wang et al., 2013), ocean (DeLong, 2009; Metcalf et al., 2012; Walsh et al., 2009), and soils (Fierer et al., 2013; Guan et al., 2013; Mackelprang et al., 2011). However, metagenomic information of full-scale A2O nitrogen and phosphorus removal reactor in municipal sewage treatment plants is still very limited. "
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    ABSTRACT: The anaerobic/anoxic/oxic (A2O) process is globally one of the widely used biological sewage treatment processes. This is the first report of a metagenomic analysis using Illumina sequencing of full-scale A2O sludge from a municipal sewage treatment plant. With more than 530,000 clean reads from different taxa and metabolic categories, the metagenome results allow us to gain insight into the functioning of the biological community of the A2O sludge. There are 51 phyla and nearly 900 genera identified from the A2O activated sludge ecosystem. Proteobacteria, Bacteroidetes, Nitrospirae and Chloroflexi are predominant phyla in the activated sludge, suggesting that these organisms play key roles in the biodegradation processes in the A2O sewage treatment system. Nitrospira, Thauera, Dechloromonas and Ignavibacterium, which have abilities to metabolize nitrogen and aromatic compounds, are most prevalent genera. The percent of nitrogen and phosphorus metabolism in the A2O sludge is 2.72% and 1.48%, respectively. In the current A2O sludge, the proportion of Candidatus Accumulibacter is 1.37%, which is several times more than that reported in a recent study of A2O sludge. Among the four processes of nitrogen metabolism, denitrification related genes had the highest number of sequences (76.74%), followed by ammonification (15.77%), nitrogen fixation (3.88%) and nitrification (3.61%). In phylum Planctomycetes, four genera (Planctomyces, Pirellula, Gemmata and Singulisphaera) are included in the top 30 abundant genera, suggesting the key role of ANAMMOX in nitrogen metabolism in the A2O sludge.
    Journal of Environmental Sciences 09/2015; 35:181-90. DOI:10.1016/j.jes.2014.12.027 · 2.00 Impact Factor
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    • "While compounds such as 2-aminoethylphosphonate (2-AEPn) (ciliatine) and 2-amino-phosphonopropionate (phosphonoalanine) had been found in many marine invertebrates (Horiguchi, 1984; Ternan et al., 1998), evidence of the occurrence of MPn had remained elusive. Recently, however, Metcalf et al. (2012) have shown that the abundant marine archaeon Nitrosopumilus maritimus encodes a novel pathway of MPn biosynthesis and produces an exopolysaccharide containing MPn esters (Metcalf et al., 2012). In addition, genes similar to those encoding MPn biosynthesis in N. maritimus were found to be relatively abundant in the planktonic marine microbial gene pool and were found in several scaffolds of the Global Ocean Survey database. "
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    ABSTRACT: Aerobic degradation of methylphosphonate (MPn) by marine bacterioplankton has been hypothesized to contribute significantly to the ocean's methane supersaturation, yet little is known about MPn utilization by marine microbes. To identify the microbial taxa and metabolic functions associated with MPn-driven methane production we performed parallel metagenomic, metatranscriptomic, and functional screening of microcosm perturbation experiments using surface water collected in the North Pacific Subtropical Gyre. In nutrient amended microcosms containing MPn, a substrate-driven microbial succession occurred. Initially, the addition of glucose and nitrate resulted in a bloom of Vibrionales and a transcriptional profile dominated by glucose-specific PTS transport and polyhydroxyalkanoate biosynthesis. Transcripts associated with phosphorus (P) acquisition were also overrepresented and suggested that the addition of glucose and nitrate had driven the community to P depletion. At this point, a second community shift occurred characterized by the increase in C-P lyase containing microbes of the Vibrionales and Rhodobacterales orders. Transcripts associated with C-P lyase components were among the most highly expressed at the community level, and only C-P lyase clusters were recovered in a functional screen for MPn utilization, consistent with this pathway being responsible for the majority, if not all, of the methane accumulation we observed. Our results identify specific bacterioplankton taxa that can utilize MPn aerobically under conditions of P limitation using the C-P lyase pathway, and thereby elicit a significant increase in the dissolved methane concentration.
    Frontiers in Microbiology 11/2013; 4:340. DOI:10.3389/fmicb.2013.00340 · 3.99 Impact Factor
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    • "Amazingly, recent research has linked microbial metabolism of these compounds in marine environments to a significant methane production involving the cleavage of the C P bond in methylphosphonate. The estimated 4 percent of global methane production [15] [16] from this process makes it a significant contributor to global warming. The contribution of solar UV photo-oxidation of phosphonate especially in the uppermost euphotic zone of surface aquatic systems cannot be over sighted. "
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    ABSTRACT: The degradation of phosphonates in the natural environment constitutes a major route by which orthophosphate (Pi) is regenerated from organic phosphorus and recently implicated in marine methane production, with ramifications to environmental pollution issues and global climate change concerns. This work explores the application of stable oxygen isotope analysis in elucidating the C P bond cleavage mechanism(s) of phosphonates by UV photo-oxidation and for tracing their sources in the environment. The two model phosphonates used, glyphosate and phosphonoacetic acid were effectively degraded after exposure to UV irradiation. The isotope results indicate the involvement of both ambient water and atmospheric oxygen in the C P bond cleavage and generally consistent with previously posited mechanisms of UV-photon excitation reactions. A model developed to calculate the oxygen isotopic composition of the original phosphonate P-moiety, shows both synthetic phosphonates having distinctly lower values compared to naturally derived organophosphorus compounds. Such mechanistic models, based on Oisotope probing, are useful for tracing the sources and reactions of phosphonates in the environment.
    Journal of Hazardous Materials 09/2013; 260:947-954. DOI:10.1016/j.jhazmat.2013.06.057 · 4.53 Impact Factor
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