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

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.

Oxidative Stress Correlates with Wolbachia-Mediated Antiviral Protection in Wolbachia-Drosophila Associations

“…Stimulation of excess reactive oxygen species (ROS) has been reported previously in Drosophila infected by Wolbachia (23).…”

Wolbachia-Free Heteropterans Do Not Produce Defensive Chemicals or Alarm Pheromones

“…Wolbachia infection of Aedes spp. and Drosophila simulans leads to elevated levels of transcripts of genes encoding enzymes involved in the production of ROS in their host's cells (Brennan et al 2012;Pan et al 2011). This increase is similar to that seen with infections by the closely related Rickettsia bacteria, in which H 2 O 2 is formed at a level that causes host cell injury (Pan et al 2011).…”

Bacteria and antiviral immunity in insects

“…Increased reactive oxygen species corresponds with Toll pathway restriction of DENV infection and it has been suggested that Wolbachia mediates anti-DENV protection via the Toll pathway [49 ]. Excess reactive oxygen species are also stimulated in Drosophila naturally infected by Wolbachia [55]. The regulation of iron metabolism of Drosophila is altered in the presence of Wolbachia [51 ,56,57] and increases in dietary iron have been linked to an increase in oxidative stress and increased Wolbachia density [58].…”