Abstract

Since the start of synthetic fertilizer production more than a hundred years ago, the coastal ocean has been exposed to increasing nutrient loading, which has led to eutrophication and extensive algal blooms. Such hypereutrophic waters might harbor anaerobic nitrogen (N) cycling processes due to low-oxygen microniches associated with abundant organic particles, but studies on nitrate reduction in coastal pelagic environments are scarce. Here, we report on 15N isotope-labeling experiments, metagenome, and RT-qPCR data from a large hypereutrophic lagoon indicating that dissimilatory nitrate reduction to ammonium (DNRA) and denitrification were active processes, even though the bulk water was fully oxygenated (> 224 µM O2). DNRA in the bottom water corresponded to 83% of whole-ecosystem DNRA (water + sediment), while denitrification was predominant in the sediment. Microbial taxa important for DNRA according to the metagenomic data were dominated by Bacteroidetes (genus Parabacteroides) and Proteobacteria (genus Wolinella), while denitrification was mainly associated with proteobacterial genera Pseudomonas, Achromobacter, and Brucella. The metagenomic and microscopy data suggest that these anaerobic processes were likely occurring in low-oxygen microniches related to extensive growth of filamentous cyanobacteria, including diazotrophic Dolichospermum and non-diazotrophic Planktothrix. By summing the total nitrate fluxes through DNRA and denitrification, it results that DNRA retains approximately one fifth (19%) of the fixed N that goes through the nitrate pool. This is noteworthy as DNRA represents thus a very important recycling mechanism for fixed N, which sustains algal proliferation and leads to further enhancement of eutrophication in these endangered ecosystems.

Highlights

  • Nitrogen (N) and phosphorus (P) are the main limiting nutrients for aquatic life (Canfield et al, 2010)

  • Since the start of synthetic fertilizer production more than a hundred years ago, the coastal ocean has been exposed to increasing nutrient loading, which has led to eutrophication and extensive algal blooms

  • Our results suggest that low oxygen or anoxic microniches associated with cyanobacteria and other algae might have been essential for dissimilatory nitrate reduction to ammonium (DNRA) and denitrification to function

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Summary

Introduction

Nitrogen (N) and phosphorus (P) are the main limiting nutrients for aquatic life (Canfield et al, 2010). Synthetic fertilizer production more than a hundred years ago, coastal environments have received increasing inputs of dissolved N and P, which have led to cultural eutrophication and subsequent phytoplankton blooms (Howarth and Marino 2006). Mineralization of such planktonic material accelerates oxygen (O2) consumption, which potentially leads to anoxia, especially in scarcely ventilated and stratified aquatic systems (Breitburg et al, 2018; Carpenter et al, 1998). The arising conditions, in which the system presents nuisance algal blooms, low visibility (< 1.5 m) and extremely high (> 50 μg L−1) chlorophyll a concentrations, are called hypereutrophic (Paerl et al, 2011)

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