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Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers.

ABSTRACT: The estuarine nitrogen cycle can be substantially altered due to anthropogenic activities resulting in increased amounts of inorganic nitrogen (mainly nitrate). In the past, denitrification was considered to be the main ecosystem process removing reactive nitrogen from the estuarine ecosystem. However, recent reports on the contribution of dissimilatory nitrate reduction to ammonium (DNRA) to nitrogen removal in these systems indicated a similar or higher importance, although the ratio between both processes remains ambiguous. Compared to denitrification, DNRA has been underexplored for the last decades and the key organisms carrying out the process in marine environments are largely unknown. Hence, as a first step to better understand the interplay between denitrification, DNRA and reduction of nitrate to nitrite in estuarine sediments, nitrogen reduction potentials were determined in sediments of the Paulina polder mudflat (Westerschelde estuary). We observed high variability in dominant nitrogen removing processes over a short distance (1.6 m), with nitrous oxide, ammonium and nitrite production rates differing significantly between all sampling sites. Denitrification occurred at all sites, DNRA was either the dominant process (two out of five sites) or absent, while nitrate reduction to nitrite was observed in most sites but never dominant. In addition, novel nitrate-to-ammonium reducers assigned to Thalassospira, Celeribacter, and Halomonas, for which DNRA was thus far unreported, were isolated, with DNRA phenotype reconfirmed through nrfA gene amplification. This study demonstrates high small scale heterogeneity among dissimilatory nitrate reduction processes in estuarine sediments and provides novel marine DNRA organisms that represent valuable alternatives to the current model organisms.

SUBMITTER: Decleyre H

PROVIDER: S-EPMC4604302 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers.

Decleyre Helen H Heylen Kim K Van Colen Carl C Willems Anne A

Frontiers in microbiology 20151014

The estuarine nitrogen cycle can be substantially altered due to anthropogenic activities resulting in increased amounts of inorganic nitrogen (mainly nitrate). In the past, denitrification was considered to be the main ecosystem process removing reactive nitrogen from the estuarine ecosystem. However, recent reports on the contribution of dissimilatory nitrate reduction to ammonium (DNRA) to nitrogen removal in these systems indicated a similar or higher importance, although the ratio between b ...[more]

PMID: 26528270

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Project description:Dissimilatory nitrate reduction to ammonium (DNRA), denitrification, anaerobic ammonium oxidation (anammox), and biological N2 fixation (BNF) can influence the nitrogen (N) use efficiency of rice production. While the effect of N application on BNF is known, little is known about its effect on NO3- partitioning between DNRA, denitrification, and anammox. Here, we investigated the effect of N application on DNRA, denitrification, anammox, and BNF and on the abundance of relevant genes in three paddy soils in Australia. Rice was grown in a glasshouse with N fertilizer (150 kg N ha-1) and without N fertilizer for 75 days, and the rhizosphere and bulk soils were collected separately for laboratory incubation and quantitative PCR analysis. Nitrogen application reduced DNRA rates by >16% in all the soils regardless of the rhizospheric zone, but it did not affect the nrfA gene abundance. Without N, the amount and proportion of NO3- reduced by DNRA (0.42 to 0.52 μg g-1 soil day-1 and 45 to 55%, respectively) were similar to or higher than the amount and proportion reduced by denitrification. However, with N the amount of NO3- reduced by DNRA (0.32 to 0.40 μg g-1 soil day-1) was 40 to 50% lower than the amount of NO3- reduced by denitrification. Denitrification loss increased by >20% with N addition and was affected by the rhizospheric zones. Nitrogen loss was minimal through anammox, while BNF added 0.02 to 0.25 μg N g-1 soil day-1 We found that DNRA plays a significant positive role in paddy soil N retention, as it accounts for up to 55% of the total NO3- reduction, but this is reduced by N application.IMPORTANCE This study provides evidence that nitrogen addition reduces nitrogen retention through DNRA and increases nitrogen loss via denitrification in a paddy soil ecosystem. DNRA is one of the major NO3- reduction processes, and it can outcompete denitrification in NO3- consumption when rice paddies are low in nitrogen. A significant level of DNRA activity in paddy soils indicates that DNRA plays an important role in retaining nitrogen by reducing NO3- availability for denitrification and leaching. Our study shows that by reducing N addition to rice paddies, there is a positive effect from reduced nitrogen loss but, more importantly, from the conversion of NO3- to NH4+, which is the favored form of mineral nitrogen for plant uptake.

Project description:Coastal zones act as a sink for riverine and atmospheric nitrogen inputs and thereby buffer the open ocean from the effects of anthropogenic activity. Recently, microbial activity in sandy permeable sediments has been identified as a dominant source of N-loss in coastal zones, namely through denitrification. Some of the highest coastal denitrification rates measured so far occur within the intertidal permeable sediments of the eutrophied Wadden Sea. Still, denitrification alone can often account for only half of the substantial nitrate (NO3-) consumption. Therefore, to investigate alternative NO3- sinks such as dissimilatory nitrate reduction to ammonium (DNRA), intracellular nitrate storage by eukaryotes and isotope equilibration effects we carried out 15NO3- amendment experiments. By considering all of these sinks in combination, we could quantify the fate of the 15NO3- added to the sediment. Denitrification was the dominant nitrate sink (50-75%), while DNRA, which recycles N to the environment accounted for 10-20% of NO3- consumption. Intriguingly, we also observed that between 20 and 40% of 15NO3- added to the incubations entered an intracellular pool of NO3- and was subsequently respired when nitrate became limiting. Eukaryotes were responsible for a large proportion of intracellular nitrate storage, and it could be shown through inhibition experiments that at least a third of the stored nitrate was subsequently also respired by eukaryotes. The environmental significance of the intracellular nitrate pool was confirmed by in situ measurements which revealed that intracellular storage can accumulate nitrate at concentrations six fold higher than the surrounding porewater. This intracellular pool is so far not considered when modeling N-loss from intertidal permeable sediments; however it can act as a reservoir for nitrate during low tide. Consequently, nitrate respiration supported by intracellular nitrate storage can add an additional 20% to previous nitrate reduction estimates in intertidal sediments, further increasing their contribution to N-loss.

Dataset Information

Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers.

Publications

Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers.

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