Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium

Extracellular polysaccharide aggregates, operationally defined as transparent exopolymeric particles (TEP), are recognized as an important conduit for carbon recycling and export in aquatic systems. Yet, the factors controlling the build-up of the TEP pool are not well characterized. Here we show that increased TEP production by Trichodesmium, an oceanic bloom-forming nitrogen-fixing (diazotrophic) cyanobacterium, is coupled with autocatalytic programmed cell death (PCD) process. We demonstrate that PCD induction, in both laboratory cultures and natural populations, is characterized by high caspase-like activity, correlates with enhanced TEP production, and occurs under iron and phosphorus starvation, as well as under high irradiance and oxidative stress. Enhanced TEP production was not observed in actively growing populations. We provide further evidence that iron is a key trigger for the induction of PCD. We demonstrate, for the first time, the concomitant enhanced build-up of the TEP pool when Trichodesmium is Fe-stressed. These results suggest a functional linkage between activation of caspases and PCD in Trichodesmium and regulation of vertical carbon and nitrogen fluxes. We hypothesize that modulation of TEP formation and its qualities by different mortality pathways could regulate the fate of phytoplankton blooms and particulate organic matter in aquatic ecosystems.