Dataset Information

Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ.

ABSTRACT:

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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.

SUBMITTER: Liu B

PROVIDER: S-EPMC4073493 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ.

Liu Binbin B Frostegård Åsa Å Bakken Lars R LR

mBio 20140624 3

<h4>Unlabelled</h4>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 ...[more]

PMID: 24961695

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Project description:Bacteria capable of reduction of nitrous oxide (N2O) to N2 separate into clade I and clade II organisms on the basis of nos operon structures and nosZ sequence features. To explore the possible ecological consequences of distinct nos clusters, the growth of bacterial isolates with either clade I (Pseudomonas stutzeri strain DCP-Ps1, Shewanella loihica strain PV-4) or clade II (Dechloromonas aromatica strain RCB, Anaeromyxobacter dehalogenans strain 2CP-C) nosZ with N2O was examined. Growth curves did not reveal trends distinguishing the clade I and clade II organisms tested; however, the growth yields of clade II organisms exceeded those of clade I organisms by 1.5- to 1.8-fold. Further, whole-cell half-saturation constants (Kss) for N2O distinguished clade I from clade II organisms. The apparent Ks values of 0.324 ± 0.078 ?M for D. aromatica and 1.34 ± 0.35 ?M for A. dehalogenans were significantly lower than the values measured for P. stutzeri (35.5 ± 9.3 ?M) and S. loihica (7.07 ± 1.13 ?M). Genome sequencing demonstrated that Dechloromonas denitrificans possessed a clade II nosZ gene, and a measured Ks of 1.01 ± 0.18 ?M for N2O was consistent with the values determined for the other clade II organisms tested. These observations provide a plausible mechanistic basis for why the relative activity of bacteria with clade I nos operons compared to that of bacteria with clade II nos operons may control N2O emissions and determine a soil's N2O sink capacity.Anthropogenic activities, in particular fertilizer application for agricultural production, increase N2O emissions to the atmosphere. N2O is a strong greenhouse gas with ozone destruction potential, and there is concern that nitrogen may become the major driver of climate change. Microbial N2O reductase (NosZ) catalyzes N2O reduction to environmentally benign dinitrogen gas and represents the major N2O sink process. The observation that bacterial groups with clade I nosZ versus those with clade II nosZ exhibit distinct affinities to N2O has implications for N2O flux models, and these distinct characteristics may provide opportunities to curb N2O emissions from relevant soil ecosystems.

Project description:The effect of standard agricultural management on the genetic heterogeneity of nitrous oxide reductase (nosZ) fragments from denitrifying prokaryotes in native and cultivated soil was explored. Thirty-six soil cores were composited from each of the two soil management conditions. nosZ gene fragments were amplified from triplicate samples, and PCR products were cloned and screened by restriction fragment length polymorphism (RFLP). The total nosZ RFLP profiles increased in similarity with soil sample size until triplicate 3-g samples produced visually identical RFLP profiles for each treatment. Large differences in total nosZ profiles were observed between the native and cultivated soils. The fragments representing major groups of clones encountered at least twice and four randomly selected clones with unique RFLP patterns were sequenced to verify nosZ identity. The sequence diversity of nosZ clones from the cultivated field was higher, and only eight patterns were found in clone libraries from both soils among the 182 distinct nosZ RFLP patterns identified from the two soils. A group of clones that comprised 32% of all clones dominated the gene library of native soil, whereas many minor groups were observed in the gene library of cultivated soil. The 95% confidence intervals of the Chao1 nonparametric richness estimator for nosZ RFLP data did not overlap, indicating that the levels of species richness are significantly different in the two soils, the cultivated soil having higher diversity. Phylogenetic analysis of deduced amino acid sequences grouped the majority of nosZ clones into an interleaved Michigan soil cluster whose cultured members are alpha-Proteobacteria. Only four nosZ sequences from cultivated soil and one from the native soil were related to sequences found in gamma-Proteobacteria. Sequences from the native field formed a distinct, closely related cluster (D(mean) = 0.16) containing 91.6% of the native clones. Clones from the cultivated field were more distantly related to each other (D(mean) = 0.26), and 65% were found outside of the cluster from the native soil, further indicating a difference in the two communities. Overall, there appears to be a relationship between use and richness, diversity, and the phylogenetic position of nosZ sequences, indicating that agricultural use of soil caused a shift to a more diverse denitrifying community.

Dataset Information

Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ.

Unlabelled

Importance

Publications

Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ.

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