Nutrient starvation and phosphonate utilization coordinate buoyancy and high-light tolerance in Trichodesmium

The formation of surface blooms by the diazotrophic cyanobacterium Trichodesmium contributes extensively to carbon and nitrogen cycling. Yet the physiological drivers governing its vertical ascent and subsequent tolerance to high surface irradiance remain obscure. By measuring sinking and floating velocities, analyzing transcriptome responses, and tracking the subcellular distribution of gas vesicles, we show that nutrient starvation is the primary trigger for vertical ascent. Specifically, iron or phosphorus depletion inhibits metabolic ballasting, disrupting the equilibrium with gas vesicle lift and driving Trichodesmium towards surface waters. Moreover, this vertical migration is safeguarded by a light-dependent metabolic "safety brake" that prevents irreversible sinking to the deep ocean. Upon reaching the surface, Trichodesmium shifts to utilizing alternative organic phosphorus sources. Particularly, the utilization of methylphosphonate (MPn) activates a distinct "surface-survival mode" characterized by the downregulation of photosynthetic activity and the relocalization of gas vesicles to form peripheral optical shields. Our findings reveal a coordinated strategy linking nutrient sensing, buoyancy regulation, and photoprotection, explaining how Trichodesmium secures its ecological success under the high irradiance of the oligotrophic surface oceans.