Mechanisms of Trichodesmium demise within the New Caledonian lagoon during the VAHINE mesocosm experiment

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.