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.