Abstract
There is increasing evidence that programmed cell death (PCD) in cyanobacteria is triggered by oxidative stress and that it contributes to the survival of the cyanobacterial population such as Microcystis aeruginosa. At the same time, microcystins (MCs) released during cell lysis have been implicated in colony formation (enabled by the release of polysaccharides) in M. aeruginosa – a strategy that allows the effect of a stressor, including grazing to be avoided or decreased. This experimental research has explored whether extracts of Daphnia magna and Daphnia cucullata (corresponding to 5, 25, 50, and 100 individuals per liter) reveal the effect on the growth, intracellular reactive oxygen species (ROS) content, lipid peroxidation, PCD, MC-LR release, and bound exopolysaccharide (EPS) level in M. aeruginosa during 7 days of exposure. As demonstrated, extracts of both daphnids induced dose-dependent growth inhibition, increase in ROS levels, lipid peroxidation, and PCD. Moreover, the release of MC-LR and an increase in the bound EPS fraction were observed in treated cultures. Generally, the greatest effects were observed under the influence of D. magna extracts. The study indicates that grazer presence can potentially trigger a series of events in the Microcystis population, with cells undergoing oxidative stress-induced PCD associated with MC release, which in turn increases EPS production by intact cells. As argued, this strategy is likely to have evolved in response to abiotic stressors, since both PCD and synthesis of MC in cyanobacteria predate the metazoan lineage. Nevertheless, it may still provide a benefit for the survival of the MC-producing M. aeruginosa population under grazer pressure.
Highlights
The interactions between cyanobacteria and zooplankton are of a complex nature
The present study investigated the effect of two daphnids of different body size, large D. magna, and small Daphnia cucullata, a widespread keystone zooplankton species, on growth, oxidative stress, MC release, programmed cell death (PCD), and the content of bound exopolysaccharides (EPS) in M. aeruginosa
The growth of cultures exposed to D. magna and D. cucullata extracts was inhibited in a dose-dependent manner (Rs = −0.98 and −0.90, respectively, for day 7; p < 0.05) with 57 and 52% decrease at day 7 following the treatment of 100 ind/L extracts, respectively, when compared to the control
Summary
The interactions between cyanobacteria and zooplankton are of a complex nature. On one hand, the increasing frequency, duration, and intensity of cyanobacterial blooms may positively select for better-adapted zooplankton that may, inter alia, express detoxification mechanisms more efficiently (Wojtal-Frankiewicz et al, 2013; Ger et al, 2014). Note that phylogenetic evidence based on the comparable levels of sequence divergence and a high degree of congruence between the MC synthetase gene 16S rRNA and rpoC1 suggests the early evolution of MC production in cyanobacteria that predates the metazoan lineage (Rantala et al, 2004). This considered, one could propose that the potential adverse effect of MCs, in the extracellular form or ingested with diet, on zooplankton such as daphnids could have undergone positive selection more recently or may represent an indirect consequence of MC biosynthesis
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