Mechanisms of <i>Trichodesmium</i> bloom demise within the New Caledonia Lagoon during the VAHINE mesocosm experiment
Abstract. The globally important marine diazotrophic cyanobacterium Trichodesmium blooms regularly in the New Caledonian lagoons (Sowthwestern Pacific). We exploited the development of a Trichodesmium bloom in the lagoon waters outside the enclosed VAHINE mesocosms to specifically investigate the cellular processes mediating its decline. Trichodesmium cells (and associated microbiota) were sampled from the time of surface accumulation to biomass demise using a series of enclosed incubations to elucidate the stressors and subcellular underpinning of rapid (~ 24 h) biomass demise and disappearance. The development and decline of Trichodesmium populations was rapid with extensive surface accumulations (blooms) appearing within 24 h on the surface waters of the lagoon. Rapid decline of > 90 % biomass after 24 h of peak accumulation was observed in p opulations that were collected and incubated under ambient conditions. Metatranscriptomic profiling of Trichodesmium biomass 8 h and 22 h after bottle incubation of surface accumulations revealed evidence for phosphorus (P) and iron (Fe) stress, with upreg ulation of genes required to increase their availability and transport. In contrast, genes responsible for nutrient storage were downregulated. Total viral abundance, assessed by SYBR-green staining and analytical flow cytometry, oscillated throughout the experiment and showed no significant relationship with Trichodesmium bloom development or demise. Enhanced caspase-specific activity and upregulation of a suite of metacaspase genes during bloom demise implicated autocatalytic programmed cell death (PCD) as the mechanistic cause. At the same time, genes associated with buoyancy and gas-vesicle production were strongly downregulated concomitant with high concentrations of transparent exopolymeric particles (TEP), greatly aiding aggregation and expediting vertical flux to depth. Our results demonstrate that the rapid demise of this high-density, Trichodesmium surface bloom over 24 h was not caused by specific lytic infection but was rather induced by PCD in response to combined nutrient and oxidative stressors.