Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by Crocosphaera watsonii

Abstract

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.

Life and death of Crocosphaera sp. in the Pacific Ocean: Fine scale predator–prey dynamics

“…comm.). Assuming Crocosphaera respires between 15% and 25% of its daily gross primary production (Inomura et al 2019), this suggests that the nitrogen fixer can sporadically support net primary production rates equivalent to the contribution of picoeukaryotes (1.58 ± 0.75 μ g C L −1 d −1 ) or Prochlorococcus (1.12 ± 0.52 μ g C L −1 d −1 ), previously measured at 5 m depth in the NPSG (Rii et al 2016).…”

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

“…To quantitatively examine the host-trichome nutrient exchange, we have developed a coarse-grained model of the Hemiaulus-Richelia symbiosis (cell flux model of DDAs: CFM-DDA) adapting relevant parts from previous CFMs [37][38][39][40][41], such as an idealized metabolic-flux network constrained by mass, energy, and electron budget. Extensive quantitative characteristics exist for this symbiosis [6], including cell volume and the number of trichomes per diatom.…”

“…The CFM-DDA model we develop here focuses on C and N metabolisms to quantify growth and N 2 fixation ( Figure 1). For most N 2 -fixing organisms, oxygen (O 2 ) metabolism is important, since O 2 damages the N 2 fixing enzyme, nitrogenase, and may control the rate of N 2 fixation [39,40,[42][43][44]. However, since the trichomes form a heterocyst, a cell with a thick glycolipid layer to minimize O 2 influx [45], we assume that intracellular O 2 is managed with normal levels of respiration [37,46].…”

Quantitative models of nitrogen-fixing organisms

“…Temporal Segregation: Crocosphaera , Cyanothece . O 2 barrier: Azotobacter (proposed [72] , predicted [53] and supported [81] , [82] ), Crocosphaera (predicted [53] , [75] ), Anabaena , Trichodesmium (predicted [83] , [84] ). Respiratory protection: Azotobacter , Crocosphaera (predicted [75] , [85] ), Trichodesmium (predicted [83] ).…”

“…respiration to reduce intracellular O 2 ) [53] , [74] . Even if there is a high O 2 flux into the cell, if the rate of respiration matches the flux, a low intracellular O 2 can be maintained [27] , [53] , [75] . Finally, there are organisms that live in low O 2 environments such as in sediments [25] , [76] , [77] and Oxygen Minimum Zones in water columns (OMZs) [78] , circumventing the O 2 problem.…”