β-cyclocitral, a novel AChE inhibitor, contributes to the defense of Microcystis aeruginosa against Daphnia grazing

J Hazard Mater. 2024 Mar 5:465:133248. doi: 10.1016/j.jhazmat.2023.133248. Epub 2023 Dec 14.

Abstract

β-cyclocitral is one of the major compounds in cyanobacterial volatile organic compound (VOCs) and can poison other aquatic organisms. To investigate the effect of β-cyclocitral on cyanobacterial-grazer interactions, Daphnia sinensis was fed Microcystis aeruginosa and exposed to β-cyclocitral. Our present study demonstrated that M. aeruginosa could significantly inhibit D. sinensis grazing. And the grazing inhibition by Microcystis aeruginosa results from the suppression of feeding rate, heart rate, thoracic limb activity and swimming speed of D. sinensis. In addition, M. aeruginosa could also induce intestinal peristalsis and emptying in D. sinensis. Interestingly, our present study found that the exposure to β-cyclocitral could mimic a range of phenotypes induced by M. aeruginosa in D. sinensis. These results suggested that M. aeruginosa could release β-cyclocitral to inhibit Daphnia grazing. To further examine the toxic mechanism of β-cyclocitral in Daphnia, several in vivo and in vitro experiments displayed that β-cyclocitral was a novel inhibitor of acetylcholinesterase (AChE). It could induce the accumulation of acetylcholine (ACh) by inhibiting AchE activity in D. sinensis. High level of endogenous Ach could inhibit feeding rate and induce intestinal peristalsis and emptying in D. sinensis.

Keywords: Acetylcholinesterase inhibitors; Cyanobacterial bloom; Daphnia sinensis; Microcystis aeruginosa; Volatile organic compounds; β-cyclocitral.

MeSH terms

  • Acetylcholinesterase
  • Aldehydes*
  • Animals
  • Cyanobacteria*
  • Daphnia
  • Diterpenes*
  • Microcystis*

Substances

  • beta-cyclocitral
  • Acetylcholinesterase
  • Diterpenes
  • Aldehydes