Ammonium uptake and dinitrogen fixation by the unicellular nanocyanobacterium Crocosphaera watsonii in nitrogen‐limited continuous cultures

Abstract

Ammonium uptake and nitrogen (N) fixation of the unicellular nanocyanobacterium Crocosphaera watsonii isolated from the western subtropical North Pacific were determined in N‐limited continuous cultures. Six steady‐state growth rates ranging from 0.10 to 0.35 d−1, corresponding to 20–75% of the maximum growth rate, were established under saturating light. Unlike other larger diazotrophs, nitrogen fixation of C. watsonii was not inhibited by ambient ammonium ranging from < 3 to 59 nmol L−1, and nitrogen fixation did not vary consistently with dilution rate and ranged from 4.4 to 12.9 fmol N cell−1 d−1, with the highest rates at intermediate dilution rates. In contrast, ammonium uptake increased significantly with increasing dilution rates over the range of 10 to 80 fmol N cell−1 d−1 and contributed 65–95% to the daily cellular N requirement. The dissolved organic nitrogen (DON) excretion increased with increasing dilution rate; however, only a small portion of assimilated nitrogen was excreted as DON. In contrast, in ammonium‐free medium, where N assimilation occurred only by dinitrogen (N2) fixation, 60% of the fixed N was excreted. Interestingly, ammonium enrichment did not increase the growth rate of C. watsonii, but cellular contents of N, phosphorus, and chlorophyll a significantly increased for most dilution rates compared with cells grown in ammonium‐free medium. C. watsonii was capable of fixing N2 while taking up ammonium at environmentally relevant low concentrations of < 3 nmol L−1, and N2 fixation was independent of nanomolar concentrations. Therefore, C. watsonii can compete with nondiazotrophic phytoplankton for ammonium in oligotrophic subtropical gyres.

Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria

“…For example, an increase in N 2 fixation has been reported for the Anthoceros-Nostoc symbioses as compared to free-living trichomes (4-and 35-fold increase relative to Anabaena and Nostoc, respectively [53]). Additionally, we find that the amount of N 2 fixation done by the trichome to support its own growth falls in a similar range to that of other non-symbiotic aquatic N 2 -fixing organisms, including filamentous Trichodesmium [32,33,54], unicellular Crocosphaera [6,34,35,55,56], and a similar heterocyst-forming trichome from freshwater environments, Nostoc [57]. The similarity of N 2 fixation rates suggests relatively conserved rates of N 2 fixation across free-living diazotrophs.…”

Diversity and Activity of Diazotrophs in Great Barrier Reef Surface Waters

“…Conversely, when DIN concentrations were ≤0.09 μM we observed the highest rates of N 2 fixation (∼68 nmol L -1 d -1 ), associated with less diverse diazotroph communities (H′ = ∼1.5), typically dominated by Trichodesmium (at 30–50% of the diazotroph assemblage). In culture, cyanobacterial and proteobacterial diazotrophs have been shown to significantly decrease N 2 fixation with increasing DIN concentrations (Knapp et al, 2012; Bentzon-Tilia et al, 2015), indicating a switch to DIN supported growth (Kustka et al, 2003; Masuda et al, 2013; Bentzon-Tilia et al, 2015), which may reduce the demand for dissolved iron (Kustka et al, 2003). However, in the environment N 2 fixation is increasingly being found to occur outside of the classical ecological niche of low DIN waters (Fernandez et al, 2011; Knapp, 2012; Farnelid et al, 2013), and can even increase in response to simulated (mesocosm) and natural (mesoscale processes) co-additions of N with other nutrients (Dekaezemacker et al, 2013; Loscher et al, 2016).…”

Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean

“…Similarly, in this study, g-24774A11 had a negative correlation with chlorophyll. The presence of ammonium inhibits the enzyme synthesis in some diazotrophs (Postgate, 1990); however, N 2 fixation in some open ocean diazotrophs appears to tolerate elevated ammonium (Dekaezemacker and Bonnet, 2011;Masuda et al, 2013). Nutrients increasing with depth with chlorophyll, especially DIN, may negatively influence fitness of g-24774A11.…”