Modeling dynamic oxygen permeability as a mechanism to mitigate oxygen-induced stresses on photosynthesis and N2 fixation in marine Trichodesmium

Abstract

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 (1.5x10-4 of O2 diffusivity in seawater) during strong photosynthesis accelerates O2 exhaust, reducing energy-consuming photorespiration by [~]40%, while low O2 permeability (1.0x10-5 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 environment, reducing photorespiration, while reduced O2 permeability later limits O2 influx from 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. HIGHLIGHTSO_LIWe developed a metabolic flux model of Trichodesmium, which resolves Dynamic cellular Permeability to O2 (DPO2). C_LIO_LIDPO2 increases N2 fixation and growth rates. C_LIO_LIDPO2 increases growth efficiency by reducing carbon wasting processes such as photorespiration and respiratory protection. C_LIO_LIDPO2, as a result, also increases iron utilization efficiency. C_LI