Symbiont‐mediated competition: Xenorhabdus bovienii confer an advantage to their nematode host Steinernema affine by killing competitor Steinernema feltiae

Abstract

Bacterial symbionts can affect several biotic interactions of their hosts, including their competition with other species. Nematodes in the genus Steinernema utilize Xenorhabdus bacterial symbionts for insect host killing and nutritional bioconversion. Here, we establish that the Xenorhabdus bovienii bacterial symbiont (Xb-Sa-78) of Steinernema affine nematodes can impact competition between S. affine and S. feltiae by a novel mechanism, directly attacking its nematode competitor. Through co-injection and natural infection assays we demonstrate the causal role of Xb-Sa-78 in the superiority of S. affine over S. feltiae nematodes during competition. Survival assays revealed that Xb-Sa-78 bacteria kill reproductive life stages of S. feltiae. Microscopy and timed infection assays indicate that Xb-Sa-78 bacteria colonize S. feltiae nematode intestines, which alters morphology of the intestine. These data suggest that Xb-Sa-78 may be an intestinal pathogen of the non-native S. feltiae nematode, although it is a nonharmful colonizer of the native nematode host, S. affine. Screening additional X. bovienii isolates revealed that intestinal infection and killing of S. feltiae is conserved among isolates from nematodes closely related to S. affine, although the underlying killing mechanisms may vary. Together, these data demonstrate that bacterial symbionts can modulate competition between their hosts, and reinforce specificity in mutualistic interactions.

A globally ubiquitous symbiont can drive experimental host evolution

“…Superspreading of Verde1 by the N2 genotype may also be an example of symbiont mediated competition, whereby a symbiont that has little cost to one host lineage imposes high costs/death on another, thus benefiting the nonsusceptible symbiont carrier (Murfin et al, 2019). Ultimately, the variable symbiont phenotypes, as well as the fitness constraints and limitations of host genetic-based defences, determined host evolutionary trajectories.…”

R-type bacteriocins of Xenorhabdus bovienii determine the outcome of interspecies competition in a natural host environment

“…In addition, by eliminating closely related strains and species that could potentially colonize the nematode, xenorhabdicin production reinforces the specificity of the symbiotic partnership. Coadaptation that establishes and maintains specificity between Xenorhabdus strains and their cognate nematode partner is an evolutionary process that involves numerous molecular products and cell biological processes [67, 68]. Xenorhabdicins may be one of the factors that help to maintain these strain-specific mutualistic associations.…”

Interactions of host‐associated multispecies bacterial communities

“…Bacteria in the genus Xenorhabdus associate with Steinernema nematodes and enable the use of insects as a source of nutrients for reproduction 81 . The bacteria detoxify the insect environment by helping suppress immunity, they liberate nutrients from the insect cadaver and serve directly as food for the nematode, and they defend the insect cadaver from scavengers and competitors through the production of natural products 82‐90 . Similarly, the symbiont Serratia symbiotica supports the nutrition of its aphid host and helps defend against pathogens 91,92 …”

“…The fitness of the pairing was inversely correlated with the phylogenetic distance of the X. bovienii strain from the native partner strain 106 . Further, some strains of X. bovienii , though beneficial for their own nematode hosts, display antagonistic toxicity toward the hosts of other X. bovienii strains 84,106 …”