Detection of phosphonoacetate degradation and <i>phnA</i> genes in soil bacteria from distinct geographical origins suggest its possible biogenic origin

Panas, Panayiotis; Ternan, Nigel G.; Dooley, James; McMullan, Geoffrey

doi:10.1111/j.1462-2920.2005.00974.x

Cited by 24 publications

(32 citation statements)

References 37 publications

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“…Indeed, our Spearman rank correlation results indicated a significant correlation between Phi and 2-PA and between Phi and 2-AEP (see Tables S2 and S3 in the supplemental material) for CH soil and PA soil, while in sediments, we observed a strong correlation only between Phi and 2-AEP (see Tables S4 and S5 in the supplemental material). Our results support the idea that there is a connection between the use of phosphonates and phosphite, possibly explained by the relationship between the genes involved in phosphonate degradation and phosphite oxidation, as suggested in previous studies (65,68,69). However, a diversity of pathways is suggested from this study, as not all strains able to use Phi could use phosphonate; the sources of the Phi are enigmatic.…”

Section: Discussionsupporting

confidence: 91%

“…Phosphonate degradation has been reported to occur via the phosphonatase pathway in marine bacteria (64), as well as in soil bacteria (65). This pathway is present in diverse bacteria, including representatives of Proteobacteria, Planctomycetes, Cyanobacteria (65), and Firmicutes (11).…”

Section: Discussionmentioning

confidence: 99%

“…This pathway is present in diverse bacteria, including representatives of Proteobacteria, Planctomycetes, Cyanobacteria (65), and Firmicutes (11). We observed phosphonatase activity in soil, but we could not detect this activity in sediments.…”

Section: Discussionmentioning

confidence: 99%

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How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

Tapia-Torres

Rodríguez-Torres

Elser

et al. 2016

Appl Environ Microbiol

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Phosphorus (P) plays a fundamental role in the physiology and biochemistry of all living things. Recent evidence indicates that organisms in the oceans can break down and use P forms in different oxidation states (e.g., ؉5, ؉3, ؉1, and ؊3); however, information is lacking for organisms from soil and sediment. The Cuatro Ciénegas Basin (CCB), Mexico, is an oligotrophic ecosystem with acute P limitation, providing a great opportunity to assess the various strategies that bacteria from soil and sediment use to obtain P. We measured the activities in sediment and soil of different exoenzymes involved in P recycling and evaluated 1,163 bacterial isolates (mainly Bacillus spp.) for their ability to use six different P substrates. DNA turned out to be a preferred substrate, comparable to a more bioavailable P source, potassium phosphate. Phosphodiesterase activity, required for DNA degradation, was observed consistently in the sampled-soil and sediment communities. A capability to use phosphite (PO 3 3؊ ) and calcium phosphate was observed mainly in sediment isolates. Phosphonates were used at a lower frequency by both soil and sediment isolates, and phosphonatase activity was detected only in soil communities. Our results revealed that soil and sediment bacteria are able to break down and use P forms in different oxidation states and contribute to ecosystem P cycling. Different strategies for P utilization were distributed between and within the different taxonomic lineages analyzed, suggesting a dynamic movement of P utilization traits among bacteria in microbial communities. IMPORTANCEPhosphorus (P) is an essential element for life found in molecules, such as DNA, cell walls, and in molecules for energy transfer, such as ATP. The Valley of Cuatro Ciénegas, Coahuila (Mexico), is a unique desert characterized by an extreme limitation of P and a great diversity of microbial life. How do bacteria in this valley manage to obtain P? We measured the availability of P and the enzymatic activity associated with P release in soil and sediment. Our results revealed that soil and sediment bacteria can break down and use P forms in different oxidation states and contribute to ecosystem P cycling. Even genetically related bacterial isolates exhibited different preferences for molecules, such as DNA, calcium phosphate, phosphite, and phosphonates, as substrates to obtain P, evidencing a distribution of roles for P utilization and suggesting a dynamic movement of P utilization traits among bacteria in microbial communities. P hosphorus (P) is an essential element for the synthesis of many biomolecules, including DNA, RNA, and ATP (1), with no substitute as a building block of life. P is also frequently limiting for a variety of biota, including vascular plants, marine and freshwater phytoplankton, aquatic and terrestrial bacteria, and herbivorous animals (2); thus, understanding how P limitation shapes ecological and evolutionary dynamics is a key step in linking levels of biological organization from genes to ecosystems.Or...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

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How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

Tapia-Torres

Rodríguez-Torres

Elser

et al. 2016

Appl Environ Microbiol

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“…We found that phnA is much more abundant than phnX throughout the water column, indicating that phosphonoacetate could be a natural product that is more abundant and ubiquitous than 2-AEP and its derivatives. The phnA gene also occurs in soil bacteria, suggesting that terrestrial bacteria could be a natural source of phosphonoacetate (Panas et al 2006). Phosphonates can be present in various biomolecules, including lipids, proteins and antibiotics (Kolowith et al 2001, Sannigrahi et al 2006.…”

Section: Discussionmentioning

confidence: 99%

Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre

Luo¹,

Zhang²,

Long³

et al. 2011

Aquat. Microb. Ecol.

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The biochemical composition of dissolved organic phosphorus (DOP) in the ocean is dominated by phosphoesters (C-O-P and C-O-P-O-C bonds), which are hydrolyzed by a diverse group of alkaline phosphatases (PhoA, PhoD, PhoX), and by phosphonates (C-P bond), which are degraded by C-P lyases and hydrolases. We designed a bioinformatics pipeline and a statistical approach to recover and analyze the alkaline phosphatase and phosphonate utilization genes from a metagenomic database derived from water samples collected from 7 depths (between 10 and 4000 m) in the oligotrophic North Pacific Subtropical Gyre. The alkaline phosphatase genes phoD and phoX were more abundant than phoA in the euphotic zone (10-130 m) and in deep waters (500-4000 m). The C-P lyase genes were most abundant in the euphotic zone at 70 m and were rare in deep water (≥500 m) where phosphate concentrations were relatively high. These observations indicate that phosphonates are utilized primarily as a phosphorus source by bacterial C-P lyases; this is consistent with the observation that C-P lyase genes are part of the pho regulon which is expressed upon phosphorus limitation. In contrast, C-P hydrolase and alkaline phosphatase genes were often more abundant in deep waters, indicating that DOP serves mainly as a carbon and energy source in phosphaterich deep waters which are depleted in bioavailable dissolved organic matter (DOM). The observed differences in depth distributions and presumed functions of C-P lyase and hydrolase genes indicate variability in the chemical composition of phosphonates between the euphotic zone and deep waters. KEY WORDS: Phosphonate hydrolase · C-P lyase · Alkaline phosphatase · Microbial phosphorus metabolismResale or republication not permitted without written consent of the publisher

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“…The organic functional group would then be released as a by-product. Thus, consumption of LMW phosphonates may result in the release of soluble organic compounds that can be used as C or energy sources (32) or of gaseous compounds that may escape consumption, such as ethane or methane (15,33).…”

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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.

show abstract

Detection of phosphonoacetate degradation and phnA genes in soil bacteria from distinct geographical origins suggest its possible biogenic origin

Cited by 24 publications

References 37 publications

How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

How To Live with Phosphorus Scarcity in Soil and Sediment: Lessons from Bacteria

Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre

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

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