Disruption of redox homeostasis leads to oxidative DNA damage in spermatocytes of Wolbachia-infected Drosophila simulans

Insect Mol Biol. 2012 Oct;21(5):510-20. doi: 10.1111/j.1365-2583.2012.01155.x. Epub 2012 Jul 26.

Abstract

Molecular interactions between symbiotic bacteria and their animal hosts are, as yet, poorly understood. The most widespread bacterial endosymbiont, Wolbachia pipientis, occurs in high density in testes of infected Drosophila simulans and causes cytoplasmic incompatibility (CI), a form of male-derived zygotic lethality. Wolbachia grow and divide within host vacuoles that generate reactive oxygen species (ROS), which in turn stimulate the up-regulation of antioxidant enzymes. These enzymes appear to protect the host from ROS-mediated damage, as there is no obvious fitness cost to Drosophila carrying Wolbachia infections. We have now determined that DNA from Wolbachia-infected mosquito Aedes albopictus (Aa23) cells shows a higher amount of the base 8-oxo-deoxyguanosine, a marker of oxidative DNA damage, than DNA from uninfected cells, and that Wolbachia infection in D. simulans is associated with an increase in DNA strand breaks in meiotic spermatocytes. Feeding exogenous antioxidants to male and female D. simulans dramatically increased Wolbachia numbers with no obvious effects on host fitness. These results suggest that ROS-induced DNA damage in sperm nuclei may contribute to the modification characteristic of CI expression in Wolbachia-infected males and that Wolbachia density is sensitive to redox balance in these flies.

MeSH terms

  • 8-Hydroxy-2'-Deoxyguanosine
  • Animals
  • Antioxidants
  • Cell Line
  • Comet Assay
  • DNA Damage*
  • Deoxyguanosine / analogs & derivatives
  • Deoxyguanosine / analysis
  • Drosophila / metabolism
  • Drosophila / microbiology*
  • Female
  • Glutathione
  • Homeostasis
  • Male
  • Oxidative Stress*
  • Spermatocytes / metabolism
  • Spermatogenesis*
  • Superoxide Dismutase / metabolism
  • Testis / metabolism
  • Testis / microbiology
  • Wolbachia / physiology*

Substances

  • Antioxidants
  • 8-Hydroxy-2'-Deoxyguanosine
  • Superoxide Dismutase
  • Deoxyguanosine
  • Glutathione