The dominant marine filamentous N₂ fixer, Trichodesmium, conducts photosynthesis and N₂ fixation during the daytime. Because N₂ fixation is sensitive to O₂, some previous studies suggested that spatial segregation of N₂ fixation and photosynthesis is essential in Trichodesmium. However, this hypothesis conflicts with some observations where all the cells contain both photosystems and the N₂-fixing enzyme nitrogenase. Here, we construct a systematic model simulating Trichodesmium metabolism, showing that the hypothetical spatial segregation is probably useless in increasing the Trichodesmium growth and N₂ fixation, unless substances can efficiently transfer among cells with low loss to the environment. The model suggests that Trichodesmium accumulates fixed carbon in the morning and uses that in respiratory protection to reduce intracellular O₂ during the mid-daytime, when photosynthesis is downregulated, allowing the occurrence of N₂ fixation. Cell membrane barrier against O₂ and alternative non-O₂ evolving electron transfer also contribute to maintaining low intracellular O₂. Our study provides a mechanism enabling N₂ fixation despite the presence of photosynthesis across Trichodesmium.