Oxidative Stress, Programmed Cell Death and Microcystin Release in Microcystis aeruginosa in Response to Daphnia Grazers

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.

Ecophysiological Aspects and sxt Genes Expression Underlying Induced Chemical Defense in STX-Producing Raphidiopsis raciborskii (Cyanobacteria) against the Zooplankter Daphnia gessneri

“…This is exemplified by the predator-mediated induction of STX production coupled to the increased resistance to grazers in A. minutum [7]. Thus, it is likely that the potential adverse effects of STXs on zooplankton have undergone positive selection more recently, as has been suggested for MCs by Rzymski et al [69].…”

Cell Death in Cyanobacteria: Current Understanding and Recommendations for a Consensus on Its Nomenclature

“…Other defense mechanisms against cyanophages include physical barriers such as natural competence and the exopolysaccharide layer ( Stucken et al, 2013 ). Interestingly, recent observations indicate the correlation between RCD and bound exopolysaccharide levels in M. aeruginosa cultures exposed to unfavorable conditions inducing oxidative stress ( Rzymski et al, 2020 ). Although in this species exopolysaccharides are known to play a role in colony formation ( Gan et al, 2012 ), they may also provide additional advantages such as protection from viral infection.…”

“…The kin selection scenario in this regard implies the quorum sensing in which the cells undergoing RCD are releasing signaling molecules to non-infected cells – whether such molecules exist is unknown. It has been however shown that extracellular microcystin promotes the expression of genes involved in exopolysaccharide synthesis in M. aeruginosa and that RCD in this cyanobacterium correlates with microcystin release, together suggesting that this metabolite may play a signaling role ( Gan et al, 2012 ; Rzymski et al, 2020 ). All in all, it remains of particular interest to investigate whether RCD may be induced by cyanophages and if it contributes to cyanobacterial fitness.…”

Algal Toxic Compounds and Their Aeroterrestrial, Airborne and other Extremophilic Producers with Attention to Soil and Plant Contamination: A Review

“…However, a lot of contradictory evidence against the sole or predominant protective role of phycotoxins was accumulated. Serious doubts come from considering the fact that cyanoprokaryotes are the most ancient phototrophs, which predate the metazoan lineage [ 83 , 98 , 99 , 100 ], and therefore, it is more likely that production of phycotoxins may be a response to specific environmental abiotic stressors [ 100 , 101 ]. For example, experiments on the influence of trace metals showed that the presence of toxin appears to give an advantage to MC-producers in the early stages of exposure to severe iron stress and may protect the cell from reactive oxygen species-induced damage [ 102 ].…”

“…The presence of AEG in recent cyanoprokaryotes suggests that the ability for its production is highly conserved, and it still can have some genetic functions [ 109 ]. Additionally, some ideas on possible function of phycotoxins as sexual attractants (pheromones) or role in gene regulation, chromosome organization, intraspecific regulation, cell differentiation in colony formations and in shaping the community composition through inter- and intra-species communication were suggested [ 31 , 97 , 100 , 107 , 110 , 111 , 112 , 113 , 114 ]. However, the strain-specific and diverse laboratory and field results obtained on the physiological aide have made it difficult to generalize [ 88 ].…”