Modeling dynamic oxygen permeability as a mechanism to mitigate oxygen-induced stresses on photosynthesis and N₂...

Trichodesmium, the predominant marine diazotrophic cyanobacterium, concurrently performs nitrogen (N₂) fixation and photosynthesis, the latter of which produces oxygen (O₂) that inhibits N₂ fixation. Hopanoid lipids in Trichodesmium may play a role in dynamically regulating membrane permeability to O₂, potentially alleviating O₂ stress on N₂ fixation. However, the physiological impacts of this dynamic permeability are not well understood. We developed a model showing that dynamically modulating membrane O₂ permeability can enhance N₂ fixation and growth of Trichodesmium by over 50%. High O₂ permeability (1.5 × 10^-4 of O₂ diffusivity in seawater) during strong photosynthesis accelerates O₂ exhaust, reducing energy-consuming photorespiration by ~40%, while low O₂ permeability (1.0 × 10^-5 diffusivity) during active N₂ fixation minimizes O₂ stress on N₂ fixation. Together, these mechanisms increase the carbon and iron use efficiencies by ~70%. Our study provides a mechanistic and quantitative framework for how dynamic O₂ permeability benefits Trichodesmium, offering insights potentially applicable to other diazotrophs.IMPORTANCETrichodesmium is a key player in marine N₂ fixation, essential for oceanic productivity and global biogeochemical cycles. However, a significant challenge arises from the concurrent photosynthetic production of O₂ during N₂ fixation, which can inhibit N₂ fixation and cause energy-wasting photorespiration. We develop a physiological model showing that Trichodesmium may dynamically regulate membrane O₂ permeability to enhance N₂ fixation and growth. The model suggests two mechanisms: elevated O₂ permeability during the early daytime of strong photosynthesis accelerates O₂ exhaust to the environment, reducing photorespiration, while reduced O₂ permeability later limits O₂ influx from the environment, lowering wasteful respiration and maintaining a low intracellular O₂ level for active N₂ fixation. These adaptations improve the efficiency of carbon and iron utilization, thereby facilitating N₂ fixation and growth in Trichodesmium. This study sheds light on how Trichodesmium and other N₂-fixing microorganisms can optimize their physiological processes in response to environmental challenges.