Modeling dynamic oxygen permeability as a mechanism to mitigate oxygen-induced stresses on photosynthesis and N2fixation in marine Trichodesmium

ABSTRACT Trichodesmium , the predominant marine diazotrophic cyanobacterium, concurrently performs nitrogen (N 2 ) fixation and photosynthesis, the latter of which produces oxygen (O 2 ) that inhibits N 2 fixation. Hopanoid lipids in Trichodesmium may play a role in dynamically regulating membrane permeability to O 2 , potentially alleviating O 2 stress on N 2 fixation. However, the physiological impacts of this dynamic permeability are not well understood. We developed a model showing that dynamically modulating membrane O 2 permeability can enhance N 2 fixation and growth of Trichodesmium by over 50%. High O 2 permeability (1.5×10 -4 of O 2 diffusivity in seawater) during strong photosynthesis accelerates O 2 exhaust, reducing energy-consuming photorespiration by ∼40%, while low O 2 permeability (1.0×10 -5 diffusivity) during active N 2 fixation minimizes O 2 stress on N 2 fixation. Together, these mechanisms increase the carbon and iron use efficiencies by ∼70%. Our study provides a mechanistic and quantitative framework for how dynamic O 2 permeability benefits Trichodesmium , offering insights potentially applicable to other diazotrophs. IMPORTANCE Trichodesmium is a key player in marine N 2 fixation, essential for oceanic productivity and global biogeochemical cycles. However, a significant challenge arises from the concurrent photosynthetic production of O 2 during N 2 fixation, which can inhibit N 2 fixation and cause energy-wasting photorespiration. We develop a physiological model showing that Trichodesmium may dynamically regulate membrane O 2 permeability to enhance N 2 fixation and growth. The model suggests two mechanisms: elevated O 2 permeability during the early daytime of strong photosynthesis accelerates O 2 exhaust to environment, reducing photorespiration, while reduced O 2 permeability later limits O 2 influx from environment, lowering wasteful respiration and maintaining a low intracellular O 2 level for active N 2 fixation. These adaptations improve the efficiency of carbon and iron utilization, thereby facilitating N 2 fixation and growth in Trichodesmium . This study sheds light on how Trichodesmium and other N 2 -fixing microorganisms can optimize their physiological processes in response to environmental challenges. HIGHLIGHTS We developed a metabolic flux model of Trichodesmium , which resolves Dynamic cellular Permeability to O 2 (DPO 2 ). DPO 2 increases N 2 fixation and growth rates. DPO 2 increases growth efficiency by reducing carbon wasting processes such as photorespiration and respiratory protection. DPO 2 , as a result, also increases iron utilization efficiency.