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Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system

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Abstract

This investigation demonstrates that programmed cell death (PCD) in a cyanobacterium, Microcystis aeruginosa, resulting from allelopathic stress induced by a submerged macrophyte, Myriophyllum spicatum, in a co-culture system. The hallmarks of PCD, caspase-3-like protease activity, DNA fragmentation, and destruction of cell ultrastructure, as well as intracellular PCD signaling radicals, reactive oxygen species (ROS), and nitric oxide (NO), were measured in M. aeruginosa cells co-cultured with M. spicatum for 7 days. The results showed a dose–response relationship between M. spicatum biomass and M. aeruginosa mortality. A caspase-3-like protease was activated and elevated from day 3. Thylakoid disintegration, cytoplasmic vacuolation, and fuzzy nuclear zone were observed by transmission electron microscopy, and distinct DNA fragmentation was detected in M. aeruginosa cells at a M. spicatum biomass of 6.0 g fresh weight (FW) L−1 during the 7 days. Allelochemicals of total phenolic compounds (TPCs) were determined in co-culture water, and the concentration increased with increasing of M. spicatum biomass and co-culture time. Compared with the level of ROS production in the control group, a significant overproduction of ROS was detected in M. aeruginosa cells in the treatment group, and this was positively correlated with TPC concentration. Furthermore, the level of intracellular NO increased with the percent mortality of M. aeruginosa. The results indicated that a PCD pathway was induced in the cyanobacterium M. aeruginosa when co-cultured with the submerged macrophyte M. spicatum.

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Acknowledgments

This research was financially supported by the National Nature Science Foundation of China (Nos. 51178452, 50909091, and 31123001), the Major Science and Technology Program for Water Pollution Control and Treatment of China 12th Five-Year Plan (No. 2012ZX07101007-005), and the State Key Laboratory of Freshwater Ecology and Biotechnology Program (No. 2013FB20). We thank Prof. Bao-Yuan Liu, Dr. Zhi-Lan Chen, Ms. Li-Ping Zhang, Zhi-Ying Lu, Xue-Mei Sun, and Fang-Jie Ge for the experimental design and paper preparation and the other members of the research group for their assistance with the work.

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  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, 430072, China

    Yan He, Qiao-Hong Zhou, Bi-Yun Liu, Long Cheng, Yun Tian, Yong-Yuan Zhang & Zhen-Bin Wu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yan He

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  1. Yan He
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Correspondence to Bi-Yun Liu or Zhen-Bin Wu.

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He, Y., Zhou, QH., Liu, BY. et al. Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system. J Appl Phycol 28, 2805–2814 (2016). https://doi.org/10.1007/s10811-016-0814-7

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  • DOI: https://doi.org/10.1007/s10811-016-0814-7

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