Response of the Ubiquitous Pelagic Diatom Thalassiosira weissflogii to Darkness and Anoxia

Abstract

Thalassiosira weissflogii, an abundant, nitrate-storing, bloom-forming diatom in the world’s oceans, can use its intracellular nitrate pool for dissimilatory nitrate reduction to ammonium (DNRA) after sudden shifts to darkness and anoxia, most likely as a survival mechanism. T. weissflogii cells that stored 4 mM 15N-nitrate consumed 1.15 (±0.25) fmol NO3 - cell-1 h-1 and simultaneously produced 1.57 (±0.21) fmol 15NH4 + cell-1 h-1 during the first 2 hours of dark/anoxic conditions. Ammonium produced from intracellular nitrate was excreted by the cells, indicating a dissimilatory rather than assimilatory pathway. Nitrite and the greenhouse gas nitrous oxide were produced at rates 2-3 orders of magnitude lower than the ammonium production rate. While DNRA activity was restricted to the first few hours of darkness and anoxia, the subsequent degradation of photopigments took weeks to months, supporting the earlier finding that diatoms resume photosynthesis even after extended exposure to darkness and anoxia. Considering the high global abundance of T. weissflogii, its production of ammonium and nitrous oxide might be of ecological importance for oceanic oxygen minimum zones and the atmosphere, respectively.

Assessing the potential of amino acid <sup>13</sup>C patterns as a carbon source tracer in marine sediments: effects of algal growth conditions and sedimentary diagenesis

“…We also note that future research is needed in terms of understanding the resistance of proteinaceous sediment material to acid hydrolysis. To answer this question, it will be particularly important to quantify proteinaceous vs. non-proteinaceous fractions of organic nitrogen in the sediment (Keil et al, 2000). The single study to date that directly compares stable isotope values of bulk sedimentary nitrogen vs. the hydrolyzable proteinaceous amino acid pool suggests that the non-proteinaceous fraction of organic nitrogen is substantial (Batista et al, 2014).…”

Intracellular Nitrate of Marine Diatoms as a Driver of Anaerobic Nitrogen Cycling in Sinking Aggregates

“…To calculate the intracellular ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$ concentration, 25 μL of the well-mixed pellet was diluted 1:10 in NaCl solution (salinity 30) plus 4% formaldehyde for diatom cell counting in a Fuchs-Rosenthal counting chamber. The remaining pellet and 100 μL of the cell-free supernatant were separately frozen at -20°C for (intracellular) ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$ analyses with an NO x analyser (CLD 66s, EcoPhysics; for details see Kamp et al, 2011, 2013). The remaining cell-free supernatant was frozen at -20°C for measurement of ${\mathrm{N}\mathrm{H}}_{\mathrm{4}}^{\mathrm{+}}$, 15 ${\mathrm{N}\mathrm{H}}_{\mathrm{4}}^{\mathrm{+}}$, and 15 ${\mathrm{N}\mathrm{O}}_{\mathrm{2}}^{\mathrm{-}}$ concentrations (for details see Kamp et al, 2013; Stief et al, 2016).…”

“…The vertical transport of intracellularly stored ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$ within sinking diatom-bacteria aggregates (Stief et al, 2016) has so far not been documented in situ . To date, diatoms are the only known ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$-storing microorganisms in marine snow, e.g., the pelagic species Skeletonema marinoi and Thalassiosira weissflogii (Kamp et al, 2011, 2013; Stief et al, 2016). Both genera are very abundant in the ocean and can contribute significantly to spring blooms and subsequent aggregate formation (Bresnan et al, 2009; Degerlund and Eilertsen, 2010; Leblanc et al, 2012).…”

“…The pelagic, centric T. weissflogii as well as the benthic, pennate Amphora coffeaeformis are known to use intracellular ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$ for dissimilatory nitrate reduction to ammonium (DNRA; ${\mathrm{N}\mathrm{O}}_{\mathrm{3}}^{\mathrm{-}}$ → ${\mathrm{N}\mathrm{O}}_{\mathrm{2}}^{\mathrm{-}}$ → ${\mathrm{N}\mathrm{H}}_{\mathrm{4}}^{\mathrm{+}}$) after sudden shifts to dark and anoxic conditions (Kamp et al, 2011, 2013, 2015), which might also hold true for S. marinoi . DNRA is an anaerobic nitrate reduction pathway, which can be used to conserve energy in the absence of O 2 (Kraft et al, 2011; Thamdrup, 2012).…”

Ecology and Evolution of Marine Diatoms and Parmales

“…This can aid survival from months to decades in dark, anoxic conditions. In a later report, Kamp et al ( 2013 ), showed that a possible survival mechanism used by the abundant oceanic species Thalassiosira weissfl ogii was the ability to use its intracellular nitrate pool for dissimilatory nitrate reduction to ammonium after sudden shifts to darkness and anoxia. Also, in stable oligotrophic conditions, such as subtropical regions and the surface layers of stratifi ed temperate pelagic regions in summer, some diatoms have developed more adaptable approaches, including symbiosis with nitrogen-fi xing cyanobacteria ( Fig.…”