Nitrogen fixation provides bioavailable nitrogen, supporting global ecosystems and influencing global cycles of other elements. It provides an additional source of nitrogen to organisms at a cost of lower growth efficiency, largely due to respiratory control of intra-cellular oxygen. Nitrogen-fixing bacteria can, however, utilize both dinitrogen gas and fixed nitrogen, decreasing energetic costs. Here we present an idealized metabolic model of the heterotrophic nitrogen fixer Azotobacter vinelandii which, constrained by laboratory data, provides quantitative predictions for conditions under which the organism uses either ammonium or nitrogen fixation, or both, as a function of the relative supply rates of carbohydrate, fixed nitrogen as well as the ambient oxygen concentration. The model reveals that the organism respires carbohydrate in excess of energetic requirements even when nitrogen fixation is inhibited and respiratory protection is not essential. The use of multiple nitrogen source expands the potential niche and range for nitrogen fixation. The model provides a quantitative framework which can be employed in ecosystem and biogeochemistry models.

Nitrogen ( $${{\rm{N}}}_{2}$$N 2 ) fixation by heterotrophic bacteria associated with sinking particles contributes to marine N cycling, but a mechanistic understanding of its regulation and significance are not available. Here we develop a mathematical model for unicellular heterotrophic bacteria growing on sinking marine particles. These bacteria can fix $${{\rm{N}}}_{2}$$N 2 under suitable environmental conditions. We find that the interactive effects of polysaccharide and polypeptide concentrations, sinking speed of particles, and surrounding $${{\rm{O}}}_{2}$$O 2 and $${{{\rm{NO}}}_{3}}^{-}$$NO 3 − concentrations determine the $${{\rm{N}}}_{2}$$N 2 fixation rate inside particles. $${{\rm{N}}}_{2}$$N 2 fixation inside sinking particles is mainly fueled by $${{{\rm{SO}}}_{4}}^{2-}$$SO 4 2 − respiration rather than $${{{\rm{NO}}}_{3}}^{-}$$NO 3 − respiration. Our model suggests that anaerobic processes, including heterotrophic $${{\rm{N}}}_{2}$$N 2 fixation, can take place in anoxic microenvironments inside sinking particles even in fully oxygenated marine waters. The modelled $${{\rm{N}}}_{2}$$N 2 fixation rates are similar to bulk rates measured in the aphotic ocean, and our study consequently suggests that particle-associated heterotrophic $${{\rm{N}}}_{2}$$N 2 fixation contributes significantly to oceanic $${{\rm{N}}}_{2}$$N 2 fixation.

The proportion of major elements in marine organic matter links cellular processes to global nutrient, oxygen and carbon cycles. Differences in the C:N:P ratios of organic matter have been observed between ocean biomes, but these patterns have yet to be quantified from the underlying small-scale physiological and ecological processes. Here we use an ecosystem model that includes adaptive resource allocation within and between ecologically distinct plankton size classes to attribute the causes of global patterns in the C:N:P ratios. We find that patterns of N:C variation are largely driven by common physiological adjustment strategies across all phytoplankton, while patterns of N:P are driven by ecological selection for taxonomic groups with different phosphorus storage capacities. Although N:C varies widely due to cellular adjustment to light and nutrients, its latitudinal gradient is modest because of depth-dependent trade-offs between nutrient and light availability. Strong latitudinal variation in N:P reflects an ecological balance favouring small plankton with lower P storage capacity in the subtropics, and larger eukaryotes with a higher cellular P storage capacity in nutrient-rich high latitudes. A weaker N:P difference between southern and northern hemispheres, and between the Atlantic and Pacific oceans, reflects differences in phosphate available for cellular storage. Despite simulating only two phytoplankton size classes, the emergent global variability of elemental ratios resembles that of all measured species, suggesting that the range of growth conditions and ecological selection sustain the observed diversity of stoichiometry among phytoplankton.

Crocosphaera is one of the major N ₂ -fixing microorganisms in the open ocean. On a global scale, the process of N ₂ fixation is important in balancing the N budget, but the factors governing the rate of N ₂ 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 O ₂ and physical factors such as temperature and light affect N ₂ fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O ₂ to protect the O ₂ -sensitive N ₂ -fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N ₂ fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.

Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.

Biological dinitrogen (N₂) fixation is a key metabolic process exclusively performed by prokaryotes, some of which are symbiotic with eukaryotes. Species of the marine haptophyte algae Braarudosphaera bigelowii harbor the N₂-fixing endosymbiotic cyanobacteria UCYN-A, which might be evolving organelle-like characteristics. We found that the size ratio between UCYN-A and their hosts is strikingly conserved across sublineages/species, which is consistent with the size relationships of organelles in this symbiosis and other species. Metabolic modeling showed that this size relationship maximizes the coordinated growth rate based on trade-offs between resource acquisition and exchange. Our findings show that the size relationships of N₂-fixing endosymbionts and organelles in unicellular eukaryotes are constrained by predictable metabolic underpinnings and that UCYN-A is, in many regards, functioning like a hypothetical N₂-fixing organelle (or nitroplast).