Bacterial symbionts can have significant impact on host fitness including by defending against predators and competitors. In this study, we describe a phenomenon in which bacterial symbionts can drive competition outcomes between members of the Steinernema genus of insect-parasitic nematodes. Soil-dwelling, microscopic Steinernema nematodes obligately associate with Xenorhabdus bacteria and together they kill insects for nutrients to develop and reproduce. Cross-pairing studies revealed that this association can be strain-specific: although Steinernema nematodes from two phylogenetic clades (I and III) associate with X. bovienii bacteria, Steinernema nematodes displayed highest fitness when paired with their cognate X. bovienii strain, with decreasing fitness correlated to increasing phylogenetic distance of the test symbiont from the native strain. Intriguingly, while clade III Steinernema nematodes paired with clade III bacterial symbionts (Xb-NCIII) produced progeny, those paired with a clade I bacterial symbiont (Xb-NCI) produced no progeny. This observation led to the hypothesis that Xb-NCI form incompatible associations with clade III Steinernema nematodes. To test this, we characterized seven additional X. bovienii strains (three Xb-NCI and four Xb-NCIII) for their interactions with clade III S. feltiae nematodes.
Results/Conclusions
Supporting our hypothesis, we found that all tested Xb-NCI, but not Xb-NCIII, killed clade III S. feltiae nematodes. In addition, Xb-NCI strains caused varied infection phenotypes and killing rates against clade III S. feltiae nematodes indicating distinct killing mechanisms. Next, we sought to identify an ecological consequence of Xb-NCI toxicity against clade III S. feltiae nematodes. To determine if this toxicity conferred a competitive advantage to clade I nematode hosts during co-infections, we injected insects with clade III S. feltiae and clade I S. affine nematodes, with or without their bacterial symbionts, and assessed the identity of the progeny produced. When clade III S. feltiae and clade I S. affine nematodes were co-injected with their bacterial symbionts, 100% of the progeny were clade I S. affine nematodes. However, when clade III S. feltiae and clade I S. affine nematodes were co-injected with only the Xb-NCIII strain, 100% of the progeny were clade III S. feltiae nematodes. These results indicate that the presence of Xb-NCI is necessary for clade I S. affine nematodes to outcompete clade III S. feltiae nematodes during co-infection. Overall, our findings show that bacterial symbionts can directly modulate competition between hosts.