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Trichodesmium is a globally important marine microbe that provides fixed nitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixation is likely regulated by iron or phosphate availability, but the extent and interaction of these controls are unclear. From metaproteomics analyses using established protein biomarkers for nutrient stress, we found that iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in the North Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was more abundant under co-stress as opposed to single nutrient stress. This is consistent with the idea that Trichodesmium has a specific physiological state during nutrient co-stress. Organic nitrogen uptake was observed and occurred simultaneously with nitrogen fixation. The quantification of the phosphate ABC transporter PstA combined with a cellular model of nutrient uptake suggested that Trichodesmium is generally confronted by the biophysical limits of membrane space and diffusion rates for iron and phosphate acquisition in the field. Colony formation may benefit nutrient acquisition from particulate and organic sources, alleviating these pressures. The results highlight that to predict the behavior of Trichodesmium, both Fe and P stress must be evaluated simultaneously.