Abstract
Intracellular nitrate storage allows microorganisms to survive fluctuating nutrient availability and anoxic conditions in aquatic ecosystems. Here we show that diatoms, ubiquitous and highly abundant microalgae, represent major cellular reservoirs of nitrate in an intertidal flat of the German Wadden Sea and are potentially involved in anaerobic nitrate respiration. Intracellular nitrate (ICNO3) was present year-round in the sediment and was spatially and temporally correlated with fucoxanthin, the marker photopigment of diatoms. Pyrosequencing of SSU rRNA genes of all domains of life confirmed that ICNO3 storage was most likely due to diatoms rather than other known nitrate-storing microorganisms (i.e., large sulfur bacteria and the eukaryotic foraminifers and gromiids). Sedimentary ICNO3 concentrations reached up to 22.3 µmol dm-3 at the sediment surface and decreased with sediment depth to negligible concentrations below 5 cm. Similarly, the ICNO3/fucoxanthin ratio and porewater nitrate (PWNO3) concentrations decreased with sediment depth, suggesting that ICNO3 of diatoms is in equilibrium with PWNO3, but is enriched relative to PWNO3 by 2-3 orders of magnitude. Cell-volume-specific ICNO3 concentrations in a diatom mat covering the sediment surface during spring were estimated at 9.3-46.7 mmol L-1. Retrieval of 18S rRNA gene sequences related to known nitrate-storing and nitrate-ammonifying diatom species suggested that diatoms in dark and anoxic sediment layers might be involved in anaerobic nitrate respiration. Due to the widespread dominance of diatoms in microphytobenthos, the total nitrate pool in coastal marine sediments may generally be at least two times larger than derived from porewater measurements and partially be recycled to ammonium.
Highlights
IntroductionNitrate serves both as a nitrogen source for assimilation, and as an electron acceptor for anaerobic respiration
In aquatic microbial communities, nitrate serves both as a nitrogen source for assimilation, and as an electron acceptor for anaerobic respiration
The seasonal and depth distribution of ICNO3 was similar to that of porewater nitrate: ICNO3 concentrations of up to 22.3 μmol dm-3 were measured at the sediment surface and negligible values were mostly reached below 5 cm sediment depth (Figure 1B)
Summary
Nitrate serves both as a nitrogen source for assimilation, and as an electron acceptor for anaerobic respiration. Microorganisms capable of anaerobic nitrate reduction (i.e., denitrification, dissimilatory nitrate reduction to ammonium (DNRA), and indirectly anaerobic ammonium oxidation (anammox)) are the major consumers of nitrate in anoxic water and sediment layers [3] For both assimilatory and dissimilatory use of nitrate, microorganisms evolved physiological mechanisms to secure nitrate supply under nitrate-limited or nitrate-fluctuating conditions, such as high-affinity nitrate transporters [4] and liquid vacuoles for ICNO3 storage [5]. Vacuolar ICNO3 storage of up to a few hundred millimolar was discovered in Foraminifera and Gromiida [12,13,14,15] These eukaryotic organisms (and possibly their endosymbionts) use their nitrate stores for denitrification to dinitrogen or nitrous oxide, which allows them to survive in anoxic sediment layers. Just like the large sulfur bacteria, Foraminifera and Gromiida are able to migrate between nitrate-containing and nitrate-free layers in the sediment
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