Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>

ABSTRACT Accumulating empirical evidence over the last 60 years has shown that the reduction of N2O to N2 is impaired by low soil pH, suggesting that liming of acid soils may reduce N2O emissions. This option has not gained much momentum in global change research, however, possibly due to limited un...

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Autores principales: Binbin Liu, Åsa Frostegård, Lars R. Bakken
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:48989ecbe5174461bf62ada3a420cf932021-11-15T15:47:39ZImpaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>10.1128/mBio.01383-142150-7511https://doaj.org/article/48989ecbe5174461bf62ada3a420cf932014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01383-14https://doaj.org/toc/2150-7511ABSTRACT Accumulating empirical evidence over the last 60 years has shown that the reduction of N2O to N2 is impaired by low soil pH, suggesting that liming of acid soils may reduce N2O emissions. This option has not gained much momentum in global change research, however, possibly due to limited understanding of why low pH interferes with N2O reductase. We hypothesized that the reason is that denitrifying organisms in soils are unable to assemble functional N2O reductase (N2OR) at low pH, as shown to be the case for the model strain Paracoccus denitrificans. We tested this by experiments with bacteria extracted from soils by density gradient centrifugation. The soils were sampled from a long-term liming experiment (soil pH 4.0, 6.1, and 8.0). The cells were incubated (stirred batches, He atmosphere) at pH levels ranging from 5.7 to 7.6, while gas kinetics (NO, N2O, and N2) and abundances of relevant denitrification genes (nirS, nirK, and nosZ) and their transcripts were monitored. Cells from the most acidic soil (pH 4.0) were unable to reduce N2O at any pH. These results warrant a closer inspection of denitrification communities of very acidic soils. Cells from the neutral soils were unable to produce functional N2OR at pH values of ≤6.1, despite significant transcription of the nosZ gene. The N2OR expressed successfully at pH 7.0, however, was functional over the entire pH range tested (5.7 to 7.6). These observations lend strong support to our hypothesis: low soil pH diminishes/prevents reduction of N2O, primarily by precluding a successful assembly of functional N2O reductase. IMPORTANCE Impaired N2O reduction in acid soils was first observed ~60 years ago, and the phenomenon has been rediscovered several times since then. The practical implication would be that the emissions of N2O from cropped soils could be controlled by soil pH management, but this option has largely been ignored till now. One reason for this could be that the mechanisms involved have remained obscure. Here, we provide compelling evidence that the primary reason is that low pH interferes with the making of the enzyme N2O reductase rather than the function of the enzyme if properly assembled. The implications are important for understanding how pH controls the kinetics of N2O and N2 production by denitrification. The improved understanding provides credibility for soil pH management as a way to mitigate N2O emissions.Binbin LiuÅsa FrostegårdLars R. BakkenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Binbin Liu
Åsa Frostegård
Lars R. Bakken
Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
description ABSTRACT Accumulating empirical evidence over the last 60 years has shown that the reduction of N2O to N2 is impaired by low soil pH, suggesting that liming of acid soils may reduce N2O emissions. This option has not gained much momentum in global change research, however, possibly due to limited understanding of why low pH interferes with N2O reductase. We hypothesized that the reason is that denitrifying organisms in soils are unable to assemble functional N2O reductase (N2OR) at low pH, as shown to be the case for the model strain Paracoccus denitrificans. We tested this by experiments with bacteria extracted from soils by density gradient centrifugation. The soils were sampled from a long-term liming experiment (soil pH 4.0, 6.1, and 8.0). The cells were incubated (stirred batches, He atmosphere) at pH levels ranging from 5.7 to 7.6, while gas kinetics (NO, N2O, and N2) and abundances of relevant denitrification genes (nirS, nirK, and nosZ) and their transcripts were monitored. Cells from the most acidic soil (pH 4.0) were unable to reduce N2O at any pH. These results warrant a closer inspection of denitrification communities of very acidic soils. Cells from the neutral soils were unable to produce functional N2OR at pH values of ≤6.1, despite significant transcription of the nosZ gene. The N2OR expressed successfully at pH 7.0, however, was functional over the entire pH range tested (5.7 to 7.6). These observations lend strong support to our hypothesis: low soil pH diminishes/prevents reduction of N2O, primarily by precluding a successful assembly of functional N2O reductase. IMPORTANCE Impaired N2O reduction in acid soils was first observed ~60 years ago, and the phenomenon has been rediscovered several times since then. The practical implication would be that the emissions of N2O from cropped soils could be controlled by soil pH management, but this option has largely been ignored till now. One reason for this could be that the mechanisms involved have remained obscure. Here, we provide compelling evidence that the primary reason is that low pH interferes with the making of the enzyme N2O reductase rather than the function of the enzyme if properly assembled. The implications are important for understanding how pH controls the kinetics of N2O and N2 production by denitrification. The improved understanding provides credibility for soil pH management as a way to mitigate N2O emissions.
format article
author Binbin Liu
Åsa Frostegård
Lars R. Bakken
author_facet Binbin Liu
Åsa Frostegård
Lars R. Bakken
author_sort Binbin Liu
title Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
title_short Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
title_full Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
title_fullStr Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
title_full_unstemmed Impaired Reduction of N<sub>2</sub>O to N<sub>2</sub> in Acid Soils Is Due to a Posttranscriptional Interference with the Expression of <italic toggle="yes">nosZ</italic>
title_sort impaired reduction of n<sub>2</sub>o to n<sub>2</sub> in acid soils is due to a posttranscriptional interference with the expression of <italic toggle="yes">nosz</italic>
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/48989ecbe5174461bf62ada3a420cf93
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AT larsrbakken impairedreductionofnsub2subotonsub2subinacidsoilsisduetoaposttranscriptionalinterferencewiththeexpressionofitalictoggleyesnoszitalic
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