The overlooked toxicity of environmentally persistent free radicals (EPFRs) induced by anthracene transformation to earthworms (Eisenia fetida)

Sci Total Environ. 2022 Dec 20:853:158571. doi: 10.1016/j.scitotenv.2022.158571. Epub 2022 Sep 6.

Abstract

Environmentally persistent free radicals (EPFRs) as intermediate products exist widely in the PAHs-contaminated soils, but toxicity assessment associated with EPFRs for terrestrial invertebrates remains unclear. Using the model organism Eisenia fetida, we compared the adverse effects among anthracene (ANT), anthraquinone (ANQ), and EPFRs induced by ANT transformation on clay surfaces. Our results showed that EPFRs-exposed earthworms experienced histopathological damage, which was more severe than ANT and ANQ-exposed earthworms. The source of EPFRs damage was associated with the obvious dysbiosis of reactive oxygen species in earthworms. Specifically, EPFRs trigged more severe antioxidant responses and oxidative damages (e.g., membrane lipid and DNA injury) in comparison with ANT and ANQ exposure, as evidenced by the values of integrated biomarker response (IBR) following the order of EPFRs (14.5) > ANT (12.8) > ANQ (10.9). Moreover, high-throughput sequencing found that EPFRs induced dramatic changes in the composition and structure of earthworm gut microbiota, which may involve immune and metabolism dysfunction, in turn aggravated EPFRs toxicity. Overall, the obtained information highlights the more severe injury of EPFRs to terrestrial organisms, deserving more attentions for the assessment of potential risks associated with radical intermediates in PAHs-contaminated soils.

Keywords: Earthworm; Environmentally persistent free radicals; Gut microbiota; PAHs; Reactive oxygen species.

MeSH terms

  • Animals
  • Anthracenes / metabolism
  • Anthracenes / toxicity
  • Anthraquinones / metabolism
  • Antioxidants / metabolism
  • Biomarkers / metabolism
  • Clay
  • Free Radicals / chemistry
  • Membrane Lipids
  • Oligochaeta* / metabolism
  • Polycyclic Aromatic Hydrocarbons* / metabolism
  • Reactive Oxygen Species / metabolism
  • Soil / chemistry
  • Soil Pollutants* / analysis

Substances

  • Soil Pollutants
  • Reactive Oxygen Species
  • Soil
  • Clay
  • Antioxidants
  • Free Radicals
  • Polycyclic Aromatic Hydrocarbons
  • anthracene
  • Anthracenes
  • Biomarkers
  • Anthraquinones
  • Membrane Lipids