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 NO₃⁻ intracellularly. Axenic strains of benthic and pelagic diatoms that stored 11–274 mM NO₃⁻ 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 NO₃⁻ pool within 1 d. A stable-isotope labeling experiment proved that ¹⁵NO₃⁻ consumption was accompanied by the production and release of ¹⁵NH₄⁺, indicating dissimilatory nitrate reduction to ammonium (DNRA). DNRA is an anaerobic respiration process that is known mainly from prokaryotic organisms, and here shown as dissimilatory nitrate reduction pathway used by a eukaryotic phototroph. Similar to large sulfur bacteria and benthic foraminifera, diatoms may respire intracellular NO₃⁻ in sediment layers without O₂ and NO₃⁻. The rapid depletion of the intracellular NO₃⁻ storage, however, implies that diatoms use DNRA to enter a resting stage for long-term survival. Assuming that pelagic diatoms are also capable of DNRA, senescing diatoms that sink through oxygen-deficient water layers may be a significant NH₄⁺ source for anammox, the prevalent nitrogen loss pathway of oceanic oxygen minimum zones.