Crocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.
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.
Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantified. Here, we develop a coarse-grained, cellular model of the symbiosis between Hemiaulus and Richelia (one of the major DDAs), which shows that carbon (C) transfer from the diatom enables a faster growth and N2 fixation rate by the trichomes. The model predicts that the rate of N2 fixation is 5.5 times that of the hypothetical case without nitrogen (N) transfer to the host diatom. The model estimates that 25% of fixed C from the host diatom is transferred to the symbiotic trichomes to support the high rate of N2 fixation. In turn, 82% of N fixed by the trichomes ends up in the host. Modeled C fixation from the vegetative cells in the trichomes supports only one-third of their total C needs. Even if we ignore the C cost for N2 fixation and for N transfer to the host, the total C cost of the trichomes is higher than the C supply by their own photosynthesis. Having more trichomes in a single host diatom decreases the demand for N2 fixation per trichome and thus decreases their cost of C. However, even with five trichomes, which is about the highest observed for Hemiaulus and Richelia symbiosis, the model still predicts a significant C transfer from the diatom host. These results help quantitatively explain the observed high rates of growth and N2 fixation in symbiotic trichomes relative to other aquatic diazotrophs.
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