The DNRA-Denitrification Dichotomy Differentiates Nitrogen Transformation Pathways in Mountain Lake Benthic Habitats.

Carlos Palacin-Lizarbe,Jordi Catalan,Emilio O Casamayor,Lluís Camarero,Sara Hallin,Christopher M Jones,Joan Cáliz

doi:10.3389/fmicb.2019.01229

Abstract

Effects of nitrogen (N) deposition on microbially-driven processes in oligotrophic freshwater ecosystems are poorly understood. We quantified guilds in the main N-transformation pathways in benthic habitats of 11 mountain lakes along a dissolved inorganic nitrogen gradient. The genes involved in denitrification (nirS, nirK, nosZ), nitrification (archaeal and bacterial amoA), dissimilatory nitrate reduction to ammonium (DNRA, nrfA) and anaerobic ammonium oxidation (anammox, hdh) were quantified, and the bacterial 16S rRNA gene was sequenced. The dominant pathways and associated bacterial communities defined four main N-transforming clusters that differed across habitat types. DNRA dominated in the sediments, except in the upper layers of more productive lakes where nirS denitrifiers prevailed with potential N2O release. Loss as N2 was more likely in lithic biofilms, as indicated by the higher hdh and nosZ abundances. Archaeal ammonia oxidisers predominated in the isoetid rhizosphere and rocky littoral sediments, suggesting nitrifying hotspots. Overall, we observed a change in potential for reactive N recycling via DNRA to N losses via denitrification as lake productivity increases in oligotrophic mountain lakes. Thus, N deposition results in a shift in genetic potential from an internal N accumulation to an atmospheric release in the respective lake systems, with increased risk for N2O emissions from productive lakes.

Highlights

According to the planetary boundaries framework (Rockström et al, 2009), anthropogenic alteration of the nitrogen (N) cycle is one of the major challenges facing the Earth system
The correlation structure markedly simplified when standardising by the 16S rRNA copy number in each sample (Figure 2C), showing that the nrfA pool was weekly related to the rest of N-functional gene pools
The genetic potential for dissimilatory nitrate reduction to ammonium (DNRA) dominate in the deep part of the lakes and the lower sediment layers, which indicates recycling of the Nr

Summary

Introduction

According to the planetary boundaries framework (Rockström et al, 2009), anthropogenic alteration of the nitrogen (N) cycle is one of the major challenges facing the Earth system. In the context of global change, remote ecosystems — defined here as being affected by atmospheric processes rather than direct human action in catchment areas — can be informative about potential large-scale changes in the Earth system. Alpine lakes of the Northern hemisphere and subarctic regions are examples of remote ecosystems that have been exposed to increased Nr deposition during the last decades (Holtgrieve et al, 2011; Camarero, 2017), triggering a nutrient imbalance in these freshwater systems which are otherwise known to have low nutrient availability (Catalan et al, 2006). While alpine and subarctic lakes are often considered important sensors of global change (Smol, 2012), there is minimal understanding of how increased Nr availability affects microbially-driven N-cycle pathways in these ecosystems (McCrackin and Elser, 2010; Palacin-Lizarbe et al, 2018). The effect of increased N deposition on the N-cycling microbial communities, and the factors controlling their distribution are poorly understood in mountain lakes

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Discussion

Conclusion