The marine diazotrophic cyanobacterium Trichodesmium responds to elevated atmospheric CO 2 partial pressure (pCO 2 ) with higher N 2 fixation and growth rates. To unveil the underlying mechanisms, we examined the combined influence of pCO 2 (150 and 900 matm) and light (50 and 200 mmol photons m 22 s 21 ) on Trichodesmium IMS101. We expand on a complementary study that demonstrated that while elevated pCO 2 enhanced N 2 fixation and growth, oxygen evolution and carbon fixation increased mainly as a response to high light. Here, we investigated changes in the photosynthetic fluorescence parameters of photosystem II, in ratios of the photosynthetic units (photosystem I:photosystem II), and in the pool sizes of key proteins involved in the fixation of carbon and nitrogen as well as their subsequent assimilation. We show that the combined elevation in pCO 2 and light controlled the operation of the CO 2 -concentrating mechanism and enhanced protein activity without increasing their pool size. Moreover, elevated pCO 2 and high light decreased the amounts of several key proteins (NifH, PsbA, and PsaC), while amounts of AtpB and RbcL did not significantly change. Reduced investment in protein biosynthesis, without notably changing photosynthetic fluxes, could free up energy that can be reallocated to increase N 2 fixation and growth at elevated pCO 2 and light. We suggest that changes in the redox state of the photosynthetic electron transport chain and posttranslational regulation of key proteins mediate the high flexibility in resources and energy allocation in Trichodesmium. This strategy should enable Trichodesmium to flourish in future surface oceans characterized by elevated pCO 2 , higher temperatures, and high light.

The globally important marine diazotrophic cyanobacterium Trichodesmium is abundant in the New Caledonian lagoon (southwestern Pacific Ocean) during austral spring/summer. We investigated the cellular processes mediating Trichodesmium mortality from large surface accumulations (blooms) in the lagoon. Trichodesmium cells (and associated microbiota) were collected at the time of surface accumulation, enclosed under simulated ambient conditions, and sampled over time to elucidate the stressors and subcellular underpinning of rapid biomass demise (> 90 % biomass crashed within ∼ 24 h). Metatranscriptomic profiling of Trichodesmium biomass, 0, 8 and 22 h after incubations of surface accumulations, demonstrated upregulated expression of genes required to increase phosphorus (P) and iron (Fe) availability and transport, while genes responsible for nutrient storage were downregulated. Total viral abundance oscillated throughout the experiment and showed no significant relationship with the development or demise of the Trichodesmium biomass. Enhanced caspase-specific activity and upregulated expression of a suite of metacaspase genes, as the Trichodesmium biomass crashed, implied autocatalytic programmed cell death (PCD) as the mechanistic cause. Concurrently, genes associated with buoyancy and gas vesicle production were strongly downregulated concomitant with increased production and high concentrations of transparent exopolymeric particles (TEP). The rapid, PCD-mediated, decline of the Trichodesmium biomass, as we observed from our incubations, parallels mortality rates reported from Trichodesmium blooms in situ. Our results suggest that, whatever the ultimate factor, PCD-mediated death in Trichodesmium can rapidly terminate blooms, facilitate aggregation, and expedite vertical flux to depth.