Rhizobium induces DNA damage in Caenorhabditis elegans intestinal cells

Abstract

In their natural habitat of rotting fruit, the nematode Caenorhabditis elegans feeds on the complex bacterial communities that thrive in this rich growth medium. Hundreds of diverse bacterial strains cultured from such rotting fruit allow C. elegans growth and reproduction when tested individually. In screens for C. elegans responses to single bacterial strains associated with nematodes in fruit, we found that Rhizobium causes a genome instability phenotype; we observed abnormally long or fragmented intestinal nuclei due to aberrant nuclear division, or defective karyokinesis. The karyokinesis defects were restricted to intestinal cells and required close proximity between bacteria and the worm. A genetic screen for C. elegans mutations that cause the same intestinal karyokinesis defect followed by genome sequencing of the isolated mutant strains identified mutations that disrupt DNA damage repair pathways, suggesting that Rhizobium may cause DNA damage in C. elegans intestinal cells. We hypothesized that such DNA damage is caused by reactive oxygen species produced by Rhizobium and found that hydrogen peroxide added to benign Escherichia coli can cause the same intestinal karyokinesis defects in WT C. elegans. Supporting this model, free radical scavengers suppressed the Rhizobium-induced C. elegans DNA damage. Thus, Rhizobium may signal to eukaryotic hosts via reactive oxygen species, and the host may respond with DNA damage repair pathways.

Regulation of Nucleotide Metabolism and Germline Proliferation in Response to Nucleotide Imbalance and Genotoxic Stresses by EndoU Nuclease

“…The DNA bridge defects were also slightly enhanced in endu-2(À) worms treated with HU ( Figure 1H). The occurrence of DNA bridges is an indicator of chromosomal damage and has been shown to be caused by mutations in DNA damage response genes in C. elegans (Kalogeropoulos et al, 2004;Kniazeva and Ruvkun, 2019). Our results suggest that ENDU-2 is necessary for successful mitosis in many intestinal cells, which is consistent with a role for ENDU-2 in the DNA damage response.…”

Dietary and environmental factors have opposite AhR-dependent effects on C. elegans healthspan

“…Instead, different bacteria diets were shown to alter worms’ metabolic profile, with worms fed HT115 having more Glu than those fed an OP50 diet [ 39 ], likely to compensate for reduced Glu produced by the bacteria. Finally, compared to HT115 fed worms, OP50 were shown to confer sensitivity to oxidative stress possibly due to mitochondrial alteration and increased ROS production [ 39 , 71 , 75 ], thus further supporting a potential role for ROS in AHR-1 activation and/or downstream activities. It will be thus interesting to decipher the specific role of Trp, Glu and/or ROS metabolism in bacterial-AHR-1 regulation of the aging process.…”

Rhizobium-Linked Nutritional and Phytochemical Changes Under Multitrophic Functional Contexts in Sustainable Food Systems

“…Direct predation on Rhizobium cells occurs in the rhizosphere by microbivore protozoans and nematodes (Ramirez and Alexander, 1980;Postma et al, 1990;Verhagen et al, 1993;Trap et al, 2016;Jiang et al, 2017). When ingested, Rhizobium induces DNA damage in the intestinal cells of the bacterivorous nematode Caenorhabditis elegans (Kniazeva and Ruvkun, 2019). Herbivory by rhizophages belonging to various taxa that feed on leguminous roots determines the establishment and function of Rhizobium-legume symbiosis within the root nodule microbiome.…”