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<p>Harmful algal blooms (HABs) caused by <i>Microcystis aeruginosa</i> are a major global threat to the aquatic environment and public health. Allelochemicals derived from aquatic and terrestrial plants are emerging weapons for eradicating these blooms. Here, juglone outperformed the most reported allelochemicals in terms of algicidal activity against <i>M. aeruginosa</i>, with a half-maximal inhibitory concentration (IC<sub>50</sub>) of 0.078 mg/L. The algal growth suppression resulted from the activation of programmed cell death (PCD) upon juglone treatment. Ultrastructural changes of juglone-induced cyanobacterial cells were characterized by marked cytoplasmic vacuolization, as indicated by transmission electron microscopy (TEM) and scanning electron microscope (SEM). Dose- and time-dependent biochemical features of <i>M. aeruginosa</i> in response to juglone included the increase in DNA fragmentation, caspase-3-like and caspase-9-like activities, phosphatidylserine externalization and chromatin condensation. Morphological and biochemical analyses revealed two modes of cell death, including apoptotic-like and autophagic-like PCD. The juglone-induced PCD was associated with increased reactive oxygen species (ROS) and nitric oxide (NO) as potential signal molecules. The blockage of the electron flow beyond (primary quinone acceptor) <i>Q</i><sub>A</sub> at photosystem II (PSII) acceptor side mediated the generation of ROS in <i>M. aeruginosa</i> exposed to juglone. Cotreatments with sodium tungstate, a nitrate reductase (NR) inhibitor, with the juglone successfully reduced NO production, suggesting that NO production in <i>M. aeruginosa</i> cells was mainly through NR pathway. The current study sheds light on the inhibition and action mode of juglone on <i>M. aeruginosa</i> from the perspective of PCD, as well as its potential for controlling cyanobacterial blooms.</p>

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Patterns and mechanisms of programmed cell death in bloom-forming Microcystis aeruginosa induced by potent allelochemical juglone

  • 期刊论文

  • 发表日期：

    2025年12月8日

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  • Xu Yang,
  • Jinyuan Chen,
  • Ang Gao,
  • Jinting Li,
  • Yulu Hu,
  • Haiying Wang,
  • Xin Zhang

摘要

Harmful algal blooms (HABs) caused by Microcystis aeruginosa are a major global threat to the aquatic environment and public health. Allelochemicals derived from aquatic and terrestrial plants are emerging weapons for eradicating these blooms. Here, juglone outperformed the most reported allelochemicals in terms of algicidal activity against M. aeruginosa, with a half-maximal inhibitory concentration (IC50) of 0.078 mg/L. The algal growth suppression resulted from the activation of programmed cell death (PCD) upon juglone treatment. Ultrastructural changes of juglone-induced cyanobacterial cells were characterized by marked cytoplasmic vacuolization, as indicated by transmission electron microscopy (TEM) and scanning electron microscope (SEM). Dose- and time-dependent biochemical features of M. aeruginosa in response to juglone included the increase in DNA fragmentation, caspase-3-like and caspase-9-like activities, phosphatidylserine externalization and chromatin condensation. Morphological and biochemical analyses revealed two modes of cell death, including apoptotic-like and autophagic-like PCD. The juglone-induced PCD was associated with increased reactive oxygen species (ROS) and nitric oxide (NO) as potential signal molecules. The blockage of the electron flow beyond (primary quinone acceptor) QA at photosystem II (PSII) acceptor side mediated the generation of ROS in M. aeruginosa exposed to juglone. Cotreatments with sodium tungstate, a nitrate reductase (NR) inhibitor, with the juglone successfully reduced NO production, suggesting that NO production in M. aeruginosa cells was mainly through NR pathway. The current study sheds light on the inhibition and action mode of juglone on M. aeruginosa from the perspective of PCD, as well as its potential for controlling cyanobacterial blooms.