Programmed Cell Death-Like and Accompanying Release of Microcystin in Freshwater Bloom-Forming Cyanobacterium Microcystis: From Identification to Ecological Relevance

Abstract

Microcystis is the most common freshwater bloom-forming cyanobacterium. Its massive blooms not only adversely affect the functionality of aquatic ecosystems, but are also associated with the production of microcystins (MCs), a group of potent toxins that become a threat to public health when cell-bound MCs are significantly released from the dying Microcystis into the water column. Managing Microcystis blooms thus requires sufficient knowledge regarding both the cell death modes and the release of toxins. Recently, more and more studies have demonstrated the occurrence of programmed cell death-like (or apoptosis-like) events in laboratory and field samples of Microcystis. Apoptosis is a genetically controlled process that is essential for the development and survival of metazoa; however, it has been gradually realized to be an existing phenomenon playing important ecological roles in unicellular microorganisms. Here, we review the current progress and the existing knowledge gap regarding apoptosis-like death in Microcystis. Specifically, we focus first on the tools utilized to characterize the apoptosis-related biochemical and morphological features in Microcystis. We further outline various stressful stimuli that trigger the occurrence of apoptosis and discuss the potential mechanisms of apoptosis in Microcystis. We then propose a conceptual model to describe the functional coupling of apoptosis and MC in Microcystis. This model could be useful for understanding both roles of MC and apoptosis in this species. Lastly, we conclude the review by highlighting the current knowledge gap and considering the direction of future research. Overall, this review provides a recent update with respect to the knowledge of apoptosis in Microcystis and also offers a guide for future investigations of its ecology and survival strategies.

A Review on the Study of Cyanotoxins in Paleolimnological Research: Current Knowledge and Future Needs

“…These timescales imply that cyanobacterial toxins play ecological role(s) other than grazer defense, and that their toxicity towards zooplankton may only be an indirect effect of their production and release into the water column. Cyanotoxin biological function still remains a subject of debate and various hypotheses, derived mostly from experimental observations, on their potential intra-and extracellular roles have been put forward [1,[12][13][14].…”

“…The gene cluster of the MC biosynthesis pathway consists of ten genes (mcyA-J), with mcyA and mcyE used most often to identify the presence of toxin producers [47,48]. The ecological role of MCs is currently under debate, with multiple hypotheses proposed, including nutrient metabolism, iron acquisition, amelioration of oxidative stress, colony-formation, quorum-sensing, info-chemical signaling, participation in light adaptation, allelopathic interactions, and functional coupling with programmed cell death [14,[49][50][51]. Due to their toxicity, MCs are currently the most studied and monitored cyanobacterial toxins.…”

“…These timescales imply that cyanobacterial toxins play ecological role(s) other than grazer defense, and that their toxicity towards zooplankton may only be an indirect effect of their production and release into the water column. Cyanotoxin biological function still remains a subject of debate and various hypotheses, derived mostly from experimental observations, on their potential intra-and extracellular roles have been put forward [1,[12][13][14].Like the ecological role of cyanobacterial metabolites, the environmental triggers causing toxin production lack definite identification in experimental and monitoring investigations. Nutrients, frequently associated with cultural eutrophication (nitrogen and phosphorus) in freshwaters, have been identified as key drivers of toxin production [15], but cyanobacteria in selected hypereutrophic systems do not produce cyanotoxins [1].…”

In Vitro Toxicological Screening of Stable and Senescing Cultures of Aphanizomenon, Planktothrix, and Raphidiopsis

“…For example, it has been suggested that cylindrospermopsin is involved in phosphate acquisition by triggering the release of alkaline phosphatase in other phytoplankton species [34,35]. However, some toxins, such as microcystins, can be released during necrosis and stress-induced programmed cell death to mediate the survival of the remaining cell population under unfavorable conditions [36].…”

Aberrant Expressional Profiling of Known MicroRNAs in the Liver of Silver Carp (Hypophthalmichthys molitrix) Following Microcystin-LR Exposure Based on samllRNA Sequencing

“…Cyanobacterial blooms in freshwater systems can produce multiply harmful cyanotoxins, particularly microcystins (MCs), which are mainly produced by bloom-forming Microcystis aeruginosa in freshwater. MCs are a group of potent toxins that become a threat to public health when cell-bound MCs are significantly released from the dying Microcystis into the water column [3]. MCs have at least 246 variants according to their chemical structure, a heptapeptide ring [4].…”