The use of amides and other organic nitrogen sources by the phytoplankton Emiliania huxleyi

Abstract

Although dissolved organic nitrogen (DON) is beginning to be seen as a potentially important nitrogen source for phytoplankton, much remains to be learned about its components and their utilization. Emiliania huxleyi, a cosmopolitan eukaryotic phytoplankton species abundant in oligotrophic oceans and during blooms in some coastal regions, was screened for use of various DON compounds. Hypoxanthine and other purines support the nickeldependent growth of most E. huxleyi strains. Acetamide and formamide but not longer chain aliphatic amides were found to be excellent nitrogen sources for growth; other phytoplankton were also found to utilize acetamide but not formamide. In E. huxleyi, small amides are transported into the cell followed by degradation to ammonia, possibly by amide-specific enzymes. The related molecules hydroxyurea and thiourea were toxic to the cells and caused an increase in fluorescence consistent with blockage of photosystern II. This fluorescence increase was inhibited by urea and acetamide, suggesting transport of hydroxyurea, thiourea, urea, and acetamide by the same or closely related transporters.Dissolved organic nitrogen (DON) is the major chemical form of N, other than N gas, in marine waters. This pool of N includes a range of compounds whose concentrations have been measured (e.g. amino acids and urea), but is mostly composed of compounds whose identities and concentrations are poorly known (Sharp 1983;Antia et al. 1991;Hopkinson et al. 1993). Because N is thought to control primary productivity in some areas of the world's oceans, the production rates and biological availability of this pool are clearly important issues. 15N tracer experiments suggest that this pool can be rapidly produced from inorganic N additions and can be available for subsequent utilization (Bronk and Glibert 1991Bronk et al. 1994).The study of the biological utilization of DON can take several approaches. One method is the generation and use of lSN-labeled natural DON for uptake experiments (Bronk and Glibert 1993).A more reductionist approach is the characterization of the turnover times (flux and concentration) of individual known compounds added to natural samples. This second approach is limited by the range of compounds that can be chemically analyzed in seawater or are available as labeled tracers. Part of this approach is also the characterization of the metabolic capabilities of microorganisms. It has been known for some time, for example, that photosynthetic microorganisms do not rely solely on inorganic N sources (a paradigm coming out of an agricultural model; Mills 1989), but are also able to utilize organic forms of nitrogen (reviewed in Antia et al. 1991). However, a large range of organisms and a range of nitrogenous compounds and N moieties remain to be examined as sources of N for phytoplankton and other marine microbes. Just as marine AcknowledgmentsWe thank John Koke for help with media preparation and some biochemical assays and Jackie Collier, Sonya Dyhrman, and two anonymous review...

Molecular insights into the niche of harmful brown tides

“…It has also been reported to grow on small amides as a sole N source, including acetamide and, to a lesser extent, formamide . This is consistent with other studies that identified that dinoflagellates, coccolithophores and diatoms grow on acetamide, and that coccolithophores grow well on formamide (Palenik and Henson, 1997). Tag 3830, which mapped to an acetamidase/ formamidase, is upregulated in the -N library, which suggests that A. anophagefferens can break down these small amides, and that this process is regulated by N deficiency.…”

“…Finally, an acetamidase/formamidase (NCBI #: 323450867) is found in this cluster and is down-regulated 2.8-fold and 1.4-fold in the -P and P-refed treatments, respectively. In the coccolithophore Emiliania huxleyi, it was demonstrated that activities of acetamidase and formamidase increased under N deficiency (Palenik and Henson 1997). Transcriptome data showed an increase in an acetamidase/formamidase in A. anophagefferens under N-deficient conditions (Wurch et al 2011).…”

Phytoplankton community dynamics during late spring coccolithophore blooms at the continental margin of the Celtic Sea (North East Atlantic, 2006–2008)

“…Tyrrell and Taylor (1996)). Emiliania huxleyi may be well-adapted to grow in low nutrient conditions, as it has been shown to have very high affinity for phosphate, and the ability to use organic nitrogen and phosphorus sources (Palenik and Henson, 1997;Riegman et al, 2000;Benner and Passow, 2010). It is likely that conflicting results regarding the necessary nutrient conditions may have been related to the high physiological and genetic variability between E. huxleyi strains, as has been shown for e.g.…”

“…Spring phytoplankton blooms are a prominent seasonal feature of the North East Atlantic Ocean (NE Atlantic) (Henson et al, 2006) and are characterised by an intense diatom bloom followed by nanoplankton (among others: prymnesiophytes, prasinophytes and cyanobacteria) when first dissolved silicate and then other nutrients become depleted, and increasing water column stratification hinders nutrient replenishment to the euphotic zone (Joint et al, 1986;Lochte et al, 1993;Rees et al, 1999;Raitsos et al, 2006;Leblanc et al, 2009). Especially, coccolithophores are a prominent feature of the late spring bloom, and this has been attributed to their tolerance for high irradiances, lower nutrient requirements and/or ability to utilise organic nitrogen or phosphorus sources (Palenik and Henson, 1997;Leblanc et al, 2009 and references therein). Bloom termination follows when nutrient depletion depresses primary productivity and grazing and viral control catch up with algal growth (Brussaard, 2004;Calbet and Landry, 2004;Behrenfeld, 2010).…”

Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean

“…Purine metabolism was consistently a large component of haptophyte QMF (5.6-27%), an order of magnitude higher than diatoms and dinoflagellates (1-2%). Purine nucleotides may represent a source of dissolved organic nitrogen accessible to haptophytes, because haptophytes have been found to grow on purines as their sole nitrogen source (33). As the precursor for nucleic acid biosynthesis, purine uptake in the ocean has also been attributed to nucleotide salvage (34).…”