Synchronization of cell death in a dinoflagellate population is mediated by an excreted thiol protease

Abstract

Regulated programmed cell death (PCD) processes have been documented in several phytoplankton species and are hypothesized to play a role in population dynamics. However, the mechanisms leading to the coordinated collapse of phytoplankton blooms are poorly understood. We showed that the collapse of the annual bloom of Peridinium gatunense, an abundant dinoflagellate in Lake Kinneret, Israel, is initiated by CO2 limitation followed by oxidative stress that triggers a PCD-like cascade. We provide evidences that a protease excreted by senescing P. gatunense cells sensitizes younger cells to oxidative stress and may consequently trigger synchronized cell death of the population. Ageing of the P. gatunense cultures was characterized by a remarkable rise in DNA fragmentation and enhanced sensitivity to H2O2. Exposure of logarithmic phase (young) cultures to conditioning media from stationary phase (old) cells sensitized them to H2O2 and led to premature massive cell death. We detected the induction of specific extracellular protease activity, leupeptin-sensitive, in ageing cultures and in lake waters during the succession of the P. gatunense bloom. Partial purification of the conditioned media revealed that this protease activity is responsible for the higher susceptibility of young cells to oxidative stress. Inhibition of the protease activity lowered the sensitivity to oxidative stress, whereas application of papain to logarithmic phase P. gatunense cultures mimicked the effect of the spent media and enhanced cell death. We propose a novel mechanistic framework by which a population of unicellular phytoplankton orchestrates a coordinated response to stress, thereby determine the fate of its individuals.

Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana

“…Fe plays a critical role in phytoplankton growth, since it is required for photosynthetic electron transfer and reductive biosynthesis (30). Dramatic reductions in photosynthetic efficiency under Fe starvation signify uncoupled electron flow through photosystem II, ultimately leading to the production of ROS in oxygenic photoautotrophs (6), which in turn induces PCD (23,60). Indeed, we found highly elevated expression of a chloroplast-localized, Mn-SOD (64) in Fe-starved cell extracts by using Western blot analysis, diagnostic of a subcellular response to elevated ROS (48,64).…”

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

“…ROS take part in the response of diatoms to iron limitation (Thamatrakoln et al, 2012), in dinoflagellate response to CO 2 limitation and to mediate allelopathic interactions with toxic cyanobacteria (Vardi et al, 1999;Sukenik et al, 2002;Vardi et al, 2002), in response to UV radiation and photoacclimation (Rijstenbil, 2002;Janknegt et al, 2008;Li et al, 2009;Fischer et al, 2012), and as a secondary burst during oxidative stress and senescence (Vardi et al, 2007;Murik and Kaplan, 2009;Murik et al, 2014). We suggest that during the host-virus interactions, EhV subverts the cellular antioxidant and ROS metabolism for its benefit, to ensure an optimal replication cycle.…”

“…Controlled by the cellular antioxidant system, ROS is a key signaling factor that mediates acclimation responses to environmental stress conditions (Foyer and Noctor, 2003;Mittler et al, 2004;D'Autréaux and Toledano, 2007;Dangoor et al, 2012). Recent reports proposed an important role for ROS metabolism in algal response to environmental stress, such as iron limitation, allelopathy, UV stress, photo-acclimation and oxidative stress (Rijstenbil, 2002;Sukenik et al, 2002;Vardi et al, 2002Vardi et al, , 2007Janknegt et al, 2008;Li et al, 2009;Murik and Kaplan, 2009;Fischer et al, 2012;Thamatrakoln et al, 2012;Graff van Creveld et al, 2014;Murik et al, 2014). As environmental stress conditions can eventually determine the fate of large-scale oceanic blooms, ROS-mediated responses may have an impact on large biogeochemical cycles.…”

Interactions of cadmium, zinc, and phosphorus in marine Synechococcus : field uptake, physiological and proteomic studies

“…Programmed cell death has been documented in several phytoplankton species, including the dinoflagellete, Peridinium gatunense, in which an excreted thiol protease is thought to coordinate cell death in culture and in blooms in the environment (Vardi et al, 2007).…”

“…Apoptosis is the process of programmed cell death in animal systems and apoptotic processes have begun to be considered in phytoplankton (Vardi et al, 2007). If Zn is modulating oxidative stress and the cells are Zn deficient, Cd can be affecting oxidative stress, which may cause cell death.…”