Intracellular nitrate storage by diatoms can be an important nitrogen pool in freshwater and marine ecosystems

Abstract

Identifying and quantifying nitrogen pools is essential for understanding the nitrogen cycle in aquatic ecosystems. The ubiquitous diatoms represent an overlooked nitrate pool as they can accumulate nitrate intracellularly and utilize it for nitrogen assimilation, dissipation of excess photosynthetic energy, and Dissimilatory Nitrate Reduction to Ammonium (DNRA). Here, we document the global co-occurrence of diatoms and intracellular nitrate in phototrophic microbial communities in freshwater (n = 69), coastal (n = 44), and open marine (n = 4) habitats. Diatom abundance and total intracellular nitrate contents in water columns, sediments, microbial mats, and epilithic biofilms were highly significantly correlated. In contrast, diatom community composition had only a marginal influence on total intracellular nitrate contents. Nitrate concentrations inside diatom cells exceeded ambient nitrate concentrations ∼100–4000-fold. The collective intracellular nitrate pool of the diatom community accounted for <1% of total nitrate in pelagic habitats and 65–95% in benthic habitats. Accordingly, nitrate-storing diatoms are emerging as significant contributors to benthic nitrogen cycling, in particular through Dissimilatory Nitrate Reduction to Ammonium activity under anoxic conditions.

The tonoplast localized protein PtNPF1 participates in the regulation of nitrogen response in diatoms

“…Intracellular NO 3 − content strongly represents vacuolar NO 3 − content. Since high NO 3 − levels are toxic in the cytoplasm (Gerasimaitė et al ., 2014; Shebanova et al ., 2017), NO 3 − taken up from the environment is quickly assimilated and converted to nitrite (NO 2 − ) by an efficient nitrate reductase (McCarthy et al ., 2017) or stored into the vacuole (Kooistra et al ., 2007; Behrenfeld et al ., 2021; Stief et al ., 2022).…”

“…In particular, nitrate (NO 3 − ) in excess, taken up in response to immediate nutritional demands, can be accumulated inside the cell during favourable periods, a phenomenon also called ‘luxury uptake’, and can be reallocated and assimilated when environmental NO 3 − is scarce, spatially confined or temporarily unavailable (Shebanova et al ., 2017; Wang et al ., 2019; Behrenfeld et al ., 2021). This ability confers diatoms a particularly useful trait in fluctuating and oligotrophic environments (Stief et al ., 2022). For example, in dark and anoxic conditions, some diatoms can consume 84–87% of their intracellular NO 3 − pool within 1 day through the Dissimilatory NO 3 − Reduction to Ammonium (NH 4 + ), an anaerobic respiration process used by many microbes to enter a resting stage for long‐term survival (Kamp et al ., 2011).…”

“…) by an efficient nitrate reductase (McCarthy et al, 2017) or stored into the vacuole (Kooistra et al, 2007;Behrenfeld et al, 2021;Stief et al, 2022).…”

Resting cells of Skeletonema marinoi assimilate organic compounds and respire by dissimilatory nitrate reduction to ammonium in dark, anoxic conditions

“…In contrast to the sun lit layer in the upper pelagic zone, coastal sediments are generally nitrogen replete and can contain high concentrations of NO 3 − in the upper millimetres to centimetres (Christensen et al, 1989; Jensen et al, 1993; Stief et al, 2022; Vanderborght & Billed, 1975). Here, we have shown that S. marinoi resting cells perform DNRA based on external NO 3 − .…”

“…Diffusion of NO 3 − from the overlying water as well as diffusion of remineralized NH 4 + nitrified to NO 3 − under well‐oxygenated conditions provide NO 3 − to surface sediments (Seitzinger, 1988). Another large fraction of total sediment NO 3 − may additionally be found intracellularly in the vacuole of diatoms (Kamp et al, 2018; Stief et al, 2022). Thus, the upper sediment offers an environment for the resting cells to survive by carrying out DNRA when N is depleted in the water column.…”