Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules

McGrath, John W.; Chin, Jason; Quinn, John P.

doi:10.1038/nrmicro3011

Cited by 198 publications

(155 citation statements)

References 81 publications

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“…Based on our data, we cannot rule out the possibility that DSM4166 can also grow on phosphonates as a source of P for two reasons: (i) Although phosphonate degradation has been well documented in recent years (Jiang et al ., 1995; White and Metcalf, 2007; Villarreal‐Chiu et al ., 2012; McGrath et al ., 2013), bacteria capable of growing on phosphonates that do not possess any of the characterized genes/proteins have been isolated, demonstrating alternative pathways for phosphonate degradation must exist in nature (Fox and Mendz, 2006); (ii) DSM4166 possesses and expressed a number of putative phosphonate transporters (Table 1 and Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria

Lidbury

Murphy

Scanlan

et al. 2016

Environmental Microbiology

137

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SummaryBacteria that inhabit the rhizosphere of agricultural crops can have a beneficial effect on crop growth. One such mechanism is the microbial‐driven solubilization and remineralization of complex forms of phosphorus (P). It is known that bacteria secrete various phosphatases in response to low P conditions. However, our understanding of their global proteomic response to P stress is limited. Here, exoproteomic analysis of Pseudomonas putida BIRD‐1 (BIRD‐1), Pseudomonas fluorescens SBW25 and Pseudomonas stutzeri DSM4166 was performed in unison with whole‐cell proteomic analysis of BIRD‐1 grown under phosphate (Pi) replete and Pi deplete conditions. Comparative exoproteomics revealed marked heterogeneity in the exoproteomes of each Pseudomonas strain in response to Pi depletion. In addition to well‐characterized members of the PHO regulon such as alkaline phosphatases, several proteins, previously not associated with the response to Pi depletion, were also identified. These included putative nucleases, phosphotriesterases, putative phosphonate transporters and outer membrane proteins. Moreover, in BIRD‐1, mutagenesis of the master regulator, phoBR, led us to confirm the addition of several novel PHO‐dependent proteins. Our data expands knowledge of the Pseudomonas PHO regulon, including species that are frequently used as bioinoculants, opening up the potential for more efficient and complete use of soil complexed P.

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Section: Discussionmentioning

confidence: 99%

Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria

Lidbury

Murphy

Scanlan

et al. 2016

Environmental Microbiology

137

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“…Finally, 2-aminoethylphosphonate may be oxidatively converted to P i and glycine with the intermediate formation of 2-amino-1-hydroxyethylphosphonate (94,95). Accounts of these highly specific enzymes in microbial metabolism have been reported previously (96,97).…”

Section: Species Variation Of the Specificity Of C-p Lyasementioning

confidence: 99%

Utilization of Glyphosate as Phosphate Source: Biochemistry and Genetics of Bacterial Carbon-Phosphorus Lyase

Hove‐Jensen

Zechel

Jochimsen

2014

Microbiol Mol Biol Rev

185

157

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SUMMARY After several decades of use of glyphosate, the active ingredient in weed killers such as Roundup, in fields, forests, and gardens, the biochemical pathway of transformation of glyphosate phosphorus to a useful phosphorus source for microorganisms has been disclosed. Glyphosate is a member of a large group of chemicals, phosphonic acids or phosphonates, which are characterized by a carbon-phosphorus bond. This is in contrast to the general phosphorus compounds utilized and metabolized by microorganisms. Here phosphorus is found as phosphoric acid or phosphate ion, phosphoric acid esters, or phosphoric acid anhydrides. The latter compounds contain phosphorus that is bound only to oxygen. Hydrolytic, oxidative, and radical-based mechanisms for carbon-phosphorus bond cleavage have been described. This review deals with the radical-based mechanism employed by the carbon-phosphorus lyase of the carbon-phosphorus lyase pathway, which involves reactions for activation of phosphonate, carbon-phosphorus bond cleavage, and further chemical transformation before a useful phosphate ion is generated in a series of seven or eight enzyme-catalyzed reactions. The phn genes, encoding the enzymes for this pathway, are widespread among bacterial species. The processes are described with emphasis on glyphosate as a substrate. Additionally, the catabolism of glyphosate is intimately connected with that of aminomethylphosphonate, which is also treated in this review. Results of physiological and genetic analyses are combined with those of bioinformatics analyses.

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“…Low-molecular-weight (LMW) phosphonates such as MPn, ethylphosphonate, and 2-aminoethylphosphonate (2-AEP) originate from the headgroups of phosphonolipids or are linked to exopolysaccharides and are produced in all three domains of life (22)(23)(24)(25). Phosphonate biosynthetic pathways are encoded in ϳ5% of microbial genomes in freshwater environments (24), suggesting that phosphonate substrates could be available in these environments.…”

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confidence: 99%

Freshwater Bacteria Release Methane as a By-Product of Phosphorus Acquisition

Yao

Henny

Maresca

2016

Appl Environ Microbiol

103

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Freshwater lakes emit large amounts of methane, some of which is produced in oxic surface waters. Two potential pathways for aerobic methane production exist: methanogenesis in oxygenated water, which has been observed in some lakes, and demethylation of small organic molecules. Although methane is produced via demethylation in oxic marine environments, this mechanism of methane release has not yet been demonstrated in freshwater systems. Genes related to the C-P lyase pathway, which cleaves C-P bonds in phosphonate compounds, were found in a metagenomic survey of the surface water of Lake Matano, which is chronically P starved and methane rich. We demonstrate that four bacterial isolates from Lake Matano obtain P from methylphosphonate and release methane and that this activity is repressed by phosphate. We further demonstrate that expression of phnJ, which encodes the enzyme that releases methane, is higher in the presence of methylphosphonate and lower when both methylphosphonate and phosphate are added. This gene is also found in most of the metagenomic data sets from freshwater environments. These experiments link methylphosphonate degradation and methane production with gene expression and phosphate availability in freshwater organisms and suggest that some of the excess methane in the Lake Matano surface water, and in other methane-rich lakes, may be produced by P-starved bacteria. IMPORTANCEMethane is an important greenhouse gas and contributes substantially to global warming. Although freshwater environments are known to release methane into the atmosphere, estimates of the amount of methane emitted by freshwater lakes vary from 8 to 73 Tg per year. Methane emissions are difficult to predict in part because the source of the methane can vary: it is the end product of the energy-conserving pathway in methanogenic archaea, which live predominantly in anoxic sediments or waters but have also been identified in some oxic freshwater environments. More recently, methane release from small organic molecules has been observed in oxic marine environments. Here we show that demethylation of methylphosphonate may also contribute to methane release from lakes and that phosphate can repress this activity. Since lakes are typically phosphorus limited, some methane release in these environments may be a by-product of phosphorus metabolism rather than carbon or energy metabolism. Methane emissions from lakes are currently predicted using primary production, eutrophication status, extent of anoxia, and the shape and size of the lake; to improve prediction of methane emissions, phosphorus availability and sources may also need to be included in these models.

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Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules

Cited by 198 publications

References 81 publications

Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria

Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria

Utilization of Glyphosate as Phosphate Source: Biochemistry and Genetics of Bacterial Carbon-Phosphorus Lyase

Freshwater Bacteria Release Methane as a By-Product of Phosphorus Acquisition

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