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Synchronization of cell death in a dinoflagellate population is mediated by an excreted thiol protease
Author(s) -
Vardi Assaf,
Eisenstadt Doron,
Murik Omer,
BermanFrank Ilana,
Zohary Tamar,
Levine Alex,
Kaplan Aaron
Publication year - 2007
Publication title -
environmental microbiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.954
H-Index - 188
eISSN - 1462-2920
pISSN - 1462-2912
DOI - 10.1111/j.1462-2920.2006.01146.x
Subject(s) - biology , programmed cell death , population , oxidative stress , protease , microbiology and biotechnology , cysteine protease , fragmentation (computing) , dinoflagellate , apoptosis , biochemistry , botany , enzyme , ecology , demography , sociology
Summary 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 CO 2 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 H 2 O 2 . Exposure of logarithmic phase (young) cultures to conditioning media from stationary phase (old) cells sensitized them to H 2 O 2 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.