Diurnally dynamic iron allocation promotes N(2) fixation in marine dominant diazotroph Trichodesmium

Trichodesmium is the dominant photoautotrophic dinitrogen (N(2)) fixer (diazotroph) in the ocean. Iron is an important factor limiting growth of marine diazotrophs including Trichodesmium mainly because of high iron content of its N(2)-fixing enzyme, nitrogenase. However, it still lacks a quantitative understanding of how dynamic iron allocation among physiological processes acts to regulate growth and N(2) fixation in Trichodesmium. Here, we constructed a model of Trichodesmium trichome in which intracellular iron could be dynamically re-allocated in photosystems and nitrogenase during the daytime. The results demonstrate that the dynamic iron allocation enhances modeled N(2) fixation and growth rates of Trichodesmium, especially in iron-limited conditions, albeit having a marginal impact under high iron concentrations. Although the reuse of iron during a day is an apparent cause that dynamic iron allocation can benefit Trichodesmium under iron limitation, our model reveals two important mechanisms. First, the release of iron from photosystems downregulates the intracellular oxygen (O(2)) production and reduces the demand of respiratory protection, a process that Trichodesmium wastefully respires carbohydrates to create a lower O(2) window for N(2) fixation. Hence, more carbohydrates can be used in growth. Second, lower allocation of iron to nitrogenase during early daytime, a period when photosynthesis is active and intracellular O(2) is high, reduces the amount of iron that is trapped in the inactivated nitrogenase induced by O(2). This mechanism further increases the iron use efficiency in Trichodesmium. Overall, our study provides mechanistic and quantitative insight into the diurnal iron allocation that can alleviate iron limitation to Trichodesmium.