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Diatoms respire nitrate to survive dark and anoxic conditions - PubMed

  • ️Sat Jan 01 2011

Diatoms respire nitrate to survive dark and anoxic conditions

Anja Kamp et al. Proc Natl Acad Sci U S A. 2011.

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)(-) pool within 1 d. A stable-isotope labeling experiment proved that (15)NO(3)(-) consumption was accompanied by the production and release of (15)NH(4)(+), 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 NO(3)(-) in sediment layers without O(2) and NO(3)(-). The rapid depletion of the intracellular NO(3)(-) 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 NH(4)(+) source for anammox, the prevalent nitrogen loss pathway of oceanic oxygen minimum zones.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Correlation between maximum intracellular NO3− concentration and survival time under dark/anoxic conditions in the diatom species D. brightwellii (D), S. costatum (S), T. weissflogii (T), C. closterium (C), N. punctata (N), and A. coffeaeformis (A). Circles denote pelagic species, diamonds denote benthic species. Values are mean concentration ± SD of three replicates; Spearman's R and probability P for nonlinear correlations are given.

Fig. 2.
Fig. 2.

Consumption of intracellular NO3− (expressed in μmol/L of growth medium) in an axenic A. coffeaeformis culture in response to dark/anoxic conditions. Time courses of NO3− concentration in the growth medium and of the mean cell density (± SE of four repeated counts) are also shown. Dark/anoxic conditions were initiated at 0 h.

Fig. 3.
Fig. 3.

Time course of N compounds in an axenic A. coffeaeformis culture in response to dark/anoxic conditions (A) and light/oxic conditions (B). Cells were preincubated with 15NO3− (A) or 14NO3− (B) in the growth medium under light/oxic conditions. Experimental conditions were initiated at 0 h. 15NH4+* denotes isotopically labeled N compounds measured with the hypobromite assay. Intracellular NO3− concentrations are expressed in μmol/L of growth medium. Values are mean ± SD of three replicate culture tubes are shown.

Fig. 4.
Fig. 4.

Conceptual model of intracellular storage and dissimilatory reduction of NO3− by benthic and pelagic diatoms. Black arrows indicate cellular uptake or release of N compounds, black dashed arrows indicate transport of cells, and white arrows indicate physiological transition to resting stage. Block arrows on the left side and horizontal dashed line through the sediment delineate zones in which light, O2, and extracellular NO3− are present or absent. Diatom cells are stylized, with centric and pennate cells representing pelagic and benthic diatoms, respectively.

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