Diatoms respire nitrate to survive dark and anoxic conditions

Abstract

Diatoms survive in dark, anoxic sediment layers for months to decades. Our investigation reveals a correlation between the dark survival potential of marine diatoms and their ability to accumulate NO 3 − intracellularly. Axenic strains of benthic and pelagic diatoms that stored 11-274 mM NO 3 − in their cells survived for 6-28 wk. After sudden shifts to dark, anoxic conditions, the benthic diatom Amphora coffeaeformis consumed 84-87% of its intracellular NO 3 Approximately 40% of marine primary production is due to diatoms, making them key players in the global carbon cycle (1). Many diatoms take up and store NO 3 − intracellularly in concentrations of up to a few 100 mM (2-4), which exceeds ambient NO 3 − concentrations by several orders of magnitude. It is well documented that diatoms use intracellular NO 3 − for assimilatory NO 3 − reduction (2); however, the intracellular NO 3 − pool also might be used for dissimilatory NO 3 − reduction. Mass sinking of pelagic diatom blooms is triggered by nutrient depletion in the surface layer of the water column (5). However, silicate depletion, not nitrate depletion, is the prevalent environmental cue for increased sinking rates (6). Therefore, the intracellular NO 3 − pool might not be depleted in diatoms that sink from the nutrient-poor surface layer to nutrient-rich deeper layers or the sediment surface. In fact, Lomstein et al. (7) found high intracellular NO 3 − pools in phytoplankton freshly deposited on the seafloor. A considerable fraction of the settled diatoms survive for months to decades as vegetative or resting cells in dark, anoxic sediment layers, in which neither photosynthesis nor aerobic respiration can occur (8-10). Benthic diatoms experience shifts to dark, anoxic conditions due to vertical migration behavior in the sediment (11) and burial by bioturbating animals (12). The occurrence of NO 3 − -storing diatoms in deep sediment layers increases the concentration of cell-bound NO 3 − , which has potential implications for nitrogen cycling (7,(13)(14)(15). However, the energy-providing metabolism that allows diatoms to survive in dark, anoxic sediments is not known, and the fate of the intracellular NO 3 − is unclear. Dissimilatory NO 3 − reduction is common in many anaerobic prokaryotes, and was recently found in several eukaryotic taxa as well. The anaerobic protozoan Loxodes spp. respires NO 3 − to NO 2 − (16), and the two fungi Fusarium oxysporum and Cylindrocarpon tonkinense respire NO 3 − to N 2 O (17, 18). Complete denitrification of NO 3 − to N 2 has been reported for NO 3 − -storing benthic foraminiferans (19,20). Dissimilatory NO 3 − reduction also can lead to NH 4 + formation in a pathway known as dissimilatory nitrate reduction to ammonium (DNRA), a process well documented in prokaryotes, such as large sulfur bacteria (21,22). The only eukaryotes known to be capable of DNRA are fungi (23,24). DNRA is involved in anaerobic energy generation via a twostep reaction sequence: NO 3 − reduction to NO 2 − is coupled to electron transport phosphor...

Nutrient availability limits biological production in Arctic sea ice melt ponds

“…However, the large removal of NO 3 − and part of the PO 4 3− decline remain unexplained. Some diatoms have been shown to intracellularly accumulate NO 3 − concentrations up to ~275 mmol L −1 (Kamp et al 2011), and C:N ratios as low as 3.8 have been observed in nitrate replete cultures (Lomas and Gilbert 2000). This likely explains a fraction of the NO 3 − depletion during our study, as the dominating algal species were diatoms.…”

Modelling Marine Sediment Biogeochemistry: Current Knowledge Gaps, Challenges, and Some Methodological Advice for Advancement

“…This dynamic directly affects key processes in the nitrogen cycle (nitrification, denitrification, DNRA), the redox cycling of metal-oxides and metal-sulphides and thereby the mobility of metals, trace-metals, phosphorus, sulphur, and pollutants (Risgaard-Petersen et al, 1993;Fenchel and Glud, 2000;Dalsgaard, 2003). Recent investigations suggest that MPB metabolism also may directly influence nitrogen turnover through DNRA and intracellular storage of nitrate (Kamp et al, 2011). Furthermore, extensive production of exopolymeric substances by MPB can affect the permeability and erosion thresholds of sediments (Hanlon et al, 2006;Pierre et al, 2014).…”

Indirect control of the intracellular nitrate pool of intertidal sediment by the polychaete Hediste diversicolor

“…Large sulphur bacteria (Schulz & Jørgensen 2001), foraminifera (Risgaard-Petersen et al 2006, Piña-Ochoa et al 2010) and microalgae (GarciaRobledo et al 2010, Kamp et al 2011) store nitrate at millimolar concentrations, while in their direct environment, porewater nitrate is available only at micromolar concentrations. Thus, the uptake of nitrate into the cell occurs against a steep concentration gradient and costs metabolic energy (Høgslund et al 2008).…”

“…Intracellular nitrate may thus sustain nitrate-consuming processes in the sediment longer or at a higher rate than porewater nitrate. The diatoms themselves use intracellular nitrate for assimilation (Lomas & Glibert 2000), but they have also been shown to reduce it to ammonium in a dissimilatory process that is induced by dark, anoxic conditions (Kamp et al 2011). Both diatoms and intracellular nitrate were detected in anoxic sediment layers of the sediment microcosms, and thus diatoms do not entirely consume their intracellular nitrate content under dark, anoxic conditions.…”

“…In the light, the microalgae probably use intracellular nitrate for nitrogen assimilation (Lomas & Glibert 2000). If buried by macrofauna to dark and anoxic conditions, the microalgae may use their intracellular nitrate for dissimilatory nitrate reduction to ammonium to meet the energy demand for entering a resting stage for long-term survival (Kamp et al 2011). Conversely, macrofauna that feed on microphytobenthos may cause the lysis of nitrate-storing cells in the gut (Smith et al 1996).…”