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Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability.

ABSTRACT: The continuous increase of nitrous oxide (N2O) abundance in the atmosphere is a global concern. Multiple pathways of N2O production occur in soil, but their significance and dependence on oxygen (O2) availability and nitrogen (N) fertilizer source are poorly understood. We examined N2O and nitric oxide (NO) production under 21%, 3%, 1%, 0.5%, and 0% (vol/vol) O2 concentrations following urea or ammonium sulfate [(NH4)2SO4] additions in loam, clay loam, and sandy loam soils that also contained ample nitrate. The contribution of the ammonia (NH3) oxidation pathways (nitrifier nitrification, nitrifier denitrification, and nitrification-coupled denitrification) and heterotrophic denitrification (HD) to N2O production was determined in 36-h incubations in microcosms by (15)N-(18)O isotope and NH3 oxidation inhibition (by 0.01% acetylene) methods. Nitrous oxide and NO production via NH3 oxidation pathways increased as O2 concentrations decreased from 21% to 0.5%. At low (0.5% and 3%) O2 concentrations, nitrifier denitrification contributed between 34% and 66%, and HD between 34% and 50% of total N2O production. Heterotrophic denitrification was responsible for all N2O production at 0% O2. Nitrifier denitrification was the main source of N2O production from ammonical fertilizer under low O2 concentrations with urea producing more N2O than (NH4)2SO4 additions. These findings challenge established thought attributing N2O emissions from soils with high water content to HD due to presumably low O2 availability. Our results imply that management practices that increase soil aeration, e.g., reducing compaction and enhancing soil structure, together with careful selection of fertilizer sources and/or nitrification inhibitors, could decrease N2O production in agricultural soils.

SUBMITTER: Zhu X

PROVIDER: S-EPMC3631630 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability.

Zhu Xia X Burger Martin M Doane Timothy A TA Horwath William R WR

Proceedings of the National Academy of Sciences of the United States of America 20130401 16

The continuous increase of nitrous oxide (N2O) abundance in the atmosphere is a global concern. Multiple pathways of N2O production occur in soil, but their significance and dependence on oxygen (O2) availability and nitrogen (N) fertilizer source are poorly understood. We examined N2O and nitric oxide (NO) production under 21%, 3%, 1%, 0.5%, and 0% (vol/vol) O2 concentrations following urea or ammonium sulfate [(NH4)2SO4] additions in loam, clay loam, and sandy loam soils that also contained am ...[more]

PMID: 23576736

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Project description:Global atmospheric loading of the climate-active gas nitrous oxide (N2O) continues to increase. A significant proportion of anthropogenic N2O emissions arises from microbial transformation of nitrogen-based fertilizers during denitrification, making microbial N2O emissions a key target for greenhouse gas reduction strategies. The genetic, physiological, and environmental regulation of microbially mediated N2O flux is poorly understood and therefore represents a critical knowledge gap in the development of successful mitigation approaches. We have previously mapped the transcriptional landscape of the model soil-denitrifying bacterium Paracoccus denitrificans Here, we show that a single bacterial small RNA (sRNA) can control the denitrification rate of P. denitrificans by stalling denitrification at nitrite reduction to limit production of downstream pathway intermediates and N2O emissions. Overexpression of sRNA-29 downregulates nitrite reductase and limits NO and N2O production by cells. RNA sequencing (RNA-seq) analysis revealed 53 genes that are controlled by sRNA-29, one of which is a previously uncharacterized GntR-type transcriptional regulator. Overexpression of this regulator phenocopies sRNA-29 overexpression and allows us to propose a model whereby sRNA-29 enhances levels of the regulator to repress denitrification under appropriate conditions. Our identification of a new regulatory pathway controlling the core denitrification pathway in bacteria highlights the current chasm in knowledge regarding genetic regulation of this pivotal biogeochemical process, which needs to be closed to support future biological and chemical N2O mitigation strategies.IMPORTANCE N2O is an important greenhouse gas and a major cause of ozone depletion. Denitrifying bacteria play vital roles in the production and consumption of N2O in many environments. Complete denitrification consists of the conversion of a soluble N-oxyanion, nitrate (NO3 -), to an inert gaseous N-oxide, dinitrogen (N2). Incomplete denitrification can occur if conditions are prohibitive, for example, under conditions of low soil copper concentrations, leading to emission of N2O rather than N2 Although enzymatically well characterized, the genetic drivers that regulate denitrification in response to environmental and physiological cues are not fully understood. This study identified a new regulatory sRNA-based control mechanism for denitrification in the model denitrifying bacterium P. denitrificans Overexpression of this sRNA slows the rate of denitrification. This report highlights that there are gaps in understanding the regulation of this important pathway which need to be filled if strategies for N2O mitigation can be rationally and carefully developed.

Project description:Denitrifying bacteria accumulate [Formula: see text], NO, and N2O, the amounts depending on transcriptional regulation of core denitrification genes in response to O2-limiting conditions. The genes include nar, nir, nor and nosZ, encoding [Formula: see text]-, [Formula: see text]-, NO- and N2O reductase, respectively. We previously constructed a dynamic model to simulate growth and respiration in batch cultures of Paracoccus denitrificans. The observed denitrification kinetics were adequately simulated by assuming a stochastic initiation of nir-transcription in each cell with an extremely low probability (0.5% h-1), leading to product- and substrate-induced transcription of nir and nor, respectively, via NO. Thus, the model predicted cell diversification: after O2 depletion, only a small fraction was able to grow by reducing [Formula: see text]. Here we have extended the model to simulate batch cultivation with [Formula: see text], i.e., [Formula: see text], NO, N2O, and N2 kinetics, measured in a novel experiment including frequent measurements of [Formula: see text]. Pa. denitrificans reduced practically all [Formula: see text] to [Formula: see text] before initiating gas production. The [Formula: see text] production is adequately simulated by assuming stochastic nar-transcription, as that for nirS, but with a higher probability (0.035 h-1) and initiating at a higher O2 concentration. Our model assumes that all cells express nosZ, thus predicting that a majority of cells have only N2O-reductase (A), while a minority (B) has [Formula: see text]-, NO- and N2O-reductase. Population B has a higher cell-specific respiration rate than A because the latter can only use N2O produced by B. Thus, the ratio [Formula: see text] is low immediately after O2 depletion, but increases throughout the anoxic phase because B grows faster than A. As a result, the model predicts initially low but gradually increasing N2O concentration throughout the anoxic phase, as observed. The modelled cell diversification neatly explains the observed denitrification kinetics and transient intermediate accumulations. The result has major implications for understanding the relationship between genotype and phenotype in denitrification research.

Project description:Methane and ammonia have to be removed from wastewater treatment effluent in order to discharge it to receiving water bodies. A potential solution for this is a combination of simultaneous ammonia and methane oxidation by anaerobic ammonia oxidation (anammox) bacteria and nitrite/nitrate-dependent anaerobic methane oxidation (N-damo) microorganisms. When applied, these microorganisms will be exposed to oxygen, but little is known about the effect of a low concentration of oxygen on a culture containing these microorganisms. In this study, a stable coculture containing anammox and N-damo microorganisms in a laboratory scale bioreactor was established under oxygen limitation. Membrane inlet mass spectrometry (MIMS) was used to directly measure the in situ simultaneous activity of N-damo, anammox, and aerobic ammonia-oxidizing microorganisms. In addition, batch tests revealed that the bioreactor also harbored aerobic methanotrophs and anaerobic methanogens. Together with fluorescence in situ hybridization (FISH) analysis and metagenomics, these results indicate that the combination of N-damo and anammox activity under the continuous supply of limiting oxygen concentrations is feasible and can be implemented for the removal of methane and ammonia from anaerobic digester effluents. IMPORTANCE Nitrogen in wastewater leads to eutrophication of the receiving water bodies, and methane is a potent greenhouse gas; it is therefore important that these are removed from wastewater. A potential solution for the simultaneous removal of nitrogenous compounds and methane is the application of a combination of nitrite/nitrate-dependent methane oxidation (N-damo) and anaerobic ammonia oxidation (annamox). In order to do so, it is important to investigate the effect of oxygen on these two anaerobic processes. In this study, we investigate the effect of a continuous oxygen supply on the activity of an anaerobic methane- and ammonia-oxidizing coculture. The findings presented in this study are important for the potential application of these two microbial processes in wastewater treatment.

Dataset Information

Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability.

Publications

Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability.

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