Iron deficiency in axenic cultures of Trichodesmium erythraeum IMS101 led to significant declines in both nitrogen fixation rates and photochemical energy conversion efficiency, accompanied by downregulation of genes encoding the major iron-binding proteins, including psbA and psbE of photosystem II, psaA and psaC of photosystem I, petB and petC of the cytochrome b6f complex, and nifH. However, the iron-starved cultures remained viable and expression of the metalloprotein genes was partially or fully restored within 3 days following the addition of iron. Both physiological and molecular responses revealed that expression and synthesis of the nitrogen fixation and photosynthetic machinery follow the hierarchy of iron demand; that is, nitrogen fixation was far more susceptible to iron limitation than photosynthesis. Consequently, the nifH transcript exhibited a 1–2 day shorter half-life and two to three times faster degradation rate than that of the photosynthetic genes. Our results suggest that the changes in gene expression are related to the redox state in the shared photosynthetic/respiratory pathway which, when faced with short-term iron deficiency, signals Trichodesmium to selectively sacrifice nitrogen fixation to conserve iron for photosynthetic and respiratory electron transport. The observed functional and compositional alterations represent the compromises in gene expression and acclimation capacity between two basic metabolic pathways competing for iron when it is limiting.