Suppression of water-bloom cyanobacterium Microcystis aeruginosa by algaecide hydrogen peroxide maximized through programmed cell death

Zhou, Tingru; Cao, Huansheng; Zheng, Jie; Teng, Fei; Wang, Xuejian; Lou, Kai; Zhang, Xihui; Tao, Yi

doi:10.1016/j.jhazmat.2020.122394

Cited by 64 publications

(25 citation statements)

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“…The evidence of these destructive processes during RCD at EC 50 should be linked to the finding that inhibition of [D-Leu 1 ]-MC-LR biosynthesis up to 60% compared to control value was also confirmed at EC 50 . These results are in line with those reported by Zhou et al (2020) , where HP treatment for 7 days with a dose range 0.26–0.44 mM caused a total MC-LR reduction of 82–86% compared to control. This finding raises the possibility that cyanobacterial toxin could be consistently degraded in cells undergoing RCD, although not necessarily in uncontrolled ACD at high HP doses ( Zhou et al, 2020 ).…”

Section: Discussionsupporting

confidence: 93%

“…These results are in line with those reported by Zhou et al (2020) , where HP treatment for 7 days with a dose range 0.26–0.44 mM caused a total MC-LR reduction of 82–86% compared to control. This finding raises the possibility that cyanobacterial toxin could be consistently degraded in cells undergoing RCD, although not necessarily in uncontrolled ACD at high HP doses ( Zhou et al, 2020 ).…”

Section: Discussionsupporting

confidence: 93%

“…In M. aeruginosa , HP treatments lead to biochemical and morphological changes such as condensation of chromatin, cytoskeletal rearrangements with cell membrane disruption (blebbing), activation of caspases-like activities, and degradation of DNA to small fragments ( Ding et al, 2012 ; Zhou et al, 2018 ) resembling RCD subroutines described in animals. Interestingly, HP treatments in M. aeruginosa are associated with a reduced release of toxins into the surrounding medium at moderate doses (0.29 mM) ( Zhou et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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A Stochastic Characterization of Hydrogen Peroxide-Induced Regulated Cell Death in Microcystis aeruginosa

et al. 2021

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Regulated cell death (RCD) encompasses the activation of cellular pathways that initiate and execute a self-dismissal process. RCD occur over a range of stressors doses that overcome pro-survival cellular pathways, while higher doses cause excessive damage leading to passive accidental cell death (ACD). Hydrogen peroxide (HP) has been proposed as a potential tool to control harmful cyanobacterial blooms, given its capacity to remove cyanobacterial cells and oxidize cyanotoxins. HP is a source of hydroxyl radicals and is expected to induce RCD only within a limited range of concentrations. This property makes this compound very useful to better understand stress-driven RCD. In this work, we analyzed cell death in microcystin-producing Microcystis aeruginosa by means of a stochastic dose response model using a wide range of HP concentrations (0, 0.29, 1.76, 3.67, 7.35, 14.70, and 29.5 mM). We used flow cytometry and unsupervised classification to study cell viability and characterize transitional cell death phenotypes after exposing cells to HP for 48 and 72 h. Non-linear regression was used to fit experimental data to a logistic cumulative distribution function (cdf) and calculate the half maximal effective concentration (EC50). The EC50 of M. aeruginosa exposed to HP were 3.77 ± 0.26 mM and 4.26 ± 0.22 mM at 48 and 72 h, respectively. The derivative of cdf (probability density function; pdf) provided theoretical and practical demonstration that EC50 is the minimal dose required to cause RCD in 50% of cells, therefore maximizing the probability of RCD occurrence. 1.76 mM HP lead to an antioxidant stress response characterized by increased reactive oxygen species (ROS) levels and HP decomposition activity. The exposure of 3.67 mM HP induced a dose-related transition in cell death phenotype, and produced several morphological changes (a less dense stroma, distortion of the cell membrane, partial disintegration of thylakoids, extensive cytoplasmic vacuolation and highly condensed chromatin). The EC50 and the stochastic cdf and pdf together with the multidimensional transitional phenotypic analysis of single cells contribute to further characterize cell death pathways in cyanobacteria.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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A Stochastic Characterization of Hydrogen Peroxide-Induced Regulated Cell Death in Microcystis aeruginosa

et al. 2021

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“…These results suggest that mannitol may induce the increase in periplasmic space and formation of OMV, leading to cell wall disruption and intracellular matter release. H 2 O 2 treatment is also reported to cause M. aeruginosa cell shrinkage, but not to cause the perforation of cell walls ( Zhou et al, 2020 ), suggesting that mannitol and H 2 O 2 induce M. aeruginosa cell death via different processes.…”

Section: Resultsmentioning

confidence: 99%

Linear Six-Carbon Sugar Alcohols Induce Lysis of Microcystis aeruginosa NIES-298 Cells

et al. 2022

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Cyanobacterial blooms are a global concern due to their adverse effects on water quality and human health. Therefore, we examined the effects of various compounds on Microcystis aeruginosa growth. We found that Microcystis aeruginosa NIES-298 cells were lysed rapidly by linear six-carbon sugar alcohols including mannitol, galactitol, iditol, fucitol, and sorbitol, but not by other sugar alcohols. Microscopic observations revealed that mannitol treatment induced crumpled inner membrane, an increase in periplasmic space, uneven cell surface with outer membrane vesicles, disruption of membrane structures, release of intracellular matter including chlorophylls, and eventual cell lysis in strain NIES-298, which differed from the previously proposed cell death modes. Mannitol metabolism, antioxidant-mediated protection of mannitol-induced cell lysis by, and caspase-3 induction in strain NIES-298 were not observed, suggesting that mannitol may not cause organic matter accumulation, oxidative stress, and programmed cell death in M. aeruginosa. No significant transcriptional expression was induced in strain NIES-298 by mannitol treatment, indicating that cell lysis is not induced through transcriptional responses. Mannitol-induced cell lysis may be specific to strain NIES-298 and target a specific component of strain NIES-298. This study will provide a basis for controlling M. aeruginosa growth specifically by non-toxic substances.

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“…A likely possibility is that it aims to enhance the population fitness by eliminating cells that were damaged by oxidative stress. It has not been fully established whether this is also the case in cyanobacteria, including Microcystis sp., but there is an increasing body of evidence that oxidative stress induces a PCD-like process in cyanobacteria and that some of the components engaged in green algae are also present here [ 96 , 97 , 98 , 99 , 100 , 101 , 102 , 103 , 104 , 105 ].…”

Section: In-lake Treatmentsmentioning

confidence: 99%

Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems: A Comprehensive Outlook on Current and Emerging Mitigation and Control Approaches

Sukenik

2021

Microorganisms

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An intensification of toxic cyanobacteria blooms has occurred over the last three decades, severely affecting coastal and lake water quality in many parts of the world. Extensive research is being conducted in an attempt to gain a better understanding of the driving forces that alter the ecological balance in water bodies and of the biological role of the secondary metabolites, toxins included, produced by the cyanobacteria. In the long-term, such knowledge may help to develop the needed procedures to restore the phytoplankton community to the pre-toxic blooms era. In the short-term, the mission of the scientific community is to develop novel approaches to mitigate the blooms and thereby restore the ability of affected communities to enjoy coastal and lake waters. Here, we critically review some of the recently proposed, currently leading, and potentially emerging mitigation approaches in-lake novel methodologies and applications relevant to drinking-water treatment.

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Suppression of water-bloom cyanobacterium Microcystis aeruginosa by algaecide hydrogen peroxide maximized through programmed cell death

Cited by 64 publications

References 64 publications

A Stochastic Characterization of Hydrogen Peroxide-Induced Regulated Cell Death in Microcystis aeruginosa

A Stochastic Characterization of Hydrogen Peroxide-Induced Regulated Cell Death in Microcystis aeruginosa

Linear Six-Carbon Sugar Alcohols Induce Lysis of Microcystis aeruginosa NIES-298 Cells

Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems: A Comprehensive Outlook on Current and Emerging Mitigation and Control Approaches

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