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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.

SUBMITTER: Murfin KE

PROVIDER: S-EPMC6252146 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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

Murfin Kristen E KE Ginete Daren R DR Bashey Farrah F Goodrich-Blair Heidi H

Environmental microbiology 20180524

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-inj ...[more]

PMID: 29799156

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Project description:UNLABELLED:Microbial symbionts provide benefits that contribute to the ecology and fitness of host plants and animals. Therefore, the evolutionary success of plants and animals fundamentally depends on long-term maintenance of beneficial associations. Most work investigating coevolution and symbiotic maintenance has focused on species-level associations, and studies are lacking that assess the impact of bacterial strain diversity on symbiotic associations within a coevolutionary framework. Here, we demonstrate that fitness in mutualism varies depending on bacterial strain identity, and this is consistent with variation shaping phylogenetic patterns and maintenance through fitness benefits. Through genome sequencing of nine bacterial symbiont strains and cophylogenetic analysis, we demonstrate diversity among Xenorhabdus bovienii bacteria. Further, we identified cocladogenesis between Steinernema feltiae nematode hosts and their corresponding X. bovienii symbiont strains, indicating potential specificity within the association. To test the specificity, we performed laboratory crosses of nematode hosts with native and nonnative symbiont strains, which revealed that combinations with the native bacterial symbiont and closely related strains performed significantly better than those with more divergent symbionts. Through genomic analyses we also defined potential factors contributing to specificity between nematode hosts and bacterial symbionts. These results suggest that strain-level diversity (e.g., subspecies-level differences) in microbial symbionts can drive variation in the success of host-microbe associations, and this suggests that these differences in symbiotic success could contribute to maintenance of the symbiosis over an evolutionary time scale. IMPORTANCE:Beneficial symbioses between microbes and plant or animal hosts are ubiquitous, and in these associations, microbial symbionts provide key benefits to their hosts. As such, host success is fundamentally dependent on long-term maintenance of beneficial associations. Prolonged association between partners in evolutionary time is expected to result in interactions in which only specific partners can fully support symbiosis. The contribution of bacterial strain diversity on specificity and coevolution in a beneficial symbiosis remains unclear. In this study, we demonstrate that strain-level differences in fitness benefits occur in beneficial host-microbe interactions, and this variation likely shapes phylogenetic patterns and symbiotic maintenance. This highlights that symbiont contributions to host biology can vary significantly based on very-fine-scale differences among members of a microbial species. Further, this work emphasizes the need for greater phylogenetic resolution when considering the causes and consequences of host-microbe interactions.

Project description:To what extent are generalist species cohesive evolutionary units rather than a compilation of recently diverged lineages? We examine this question in the context of host specificity and geographic structure in the insect pathogen and nematode mutualist Xenorhabdus bovienii. This bacterial species partners with multiple nematode species across two clades in the genus Steinernema. We sequenced the genomes of 42 X. bovienii strains isolated from four different nematode species and three field sites within a 240-km2 region and compared them to globally available reference genomes. We hypothesized that X. bovienii would comprise several host-specific lineages, such that bacterial and nematode phylogenies would be largely congruent. Alternatively, we hypothesized that spatial proximity might be a dominant signal, as increasing geographic distance might lower shared selective pressures and opportunities for gene flow. We found partial support for both hypotheses. Isolates clustered largely by nematode host species but did not strictly match the nematode phylogeny, indicating that shifts in symbiont associations across nematode species and clades have occurred. Furthermore, both genetic similarity and gene flow decreased with geographic distance across nematode species, suggesting differentiation and constraints on gene flow across both factors, although no absolute barriers to gene flow were observed across the regional isolates. Several genes associated with biotic interactions were found to be undergoing selective sweeps within this regional population. The interactions included several insect toxins and genes implicated in microbial competition. Thus, gene flow maintains cohesiveness across host associations in this symbiont and may facilitate adaptive responses to a multipartite selective environment. IMPORTANCE Microbial populations and species are notoriously hard to delineate. We used a population genomics approach to examine the population structure and the spatial scale of gene flow in Xenorhabdus bovienii, an intriguing species that is both a specialized mutualistic symbiont of nematodes and a broadly virulent insect pathogen. We found a strong signature of nematode host association, as well as evidence for gene flow connecting isolates associated with different nematode host species and collected from distinct study sites. Furthermore, we saw signatures of selective sweeps for genes involved with nematode host associations, insect pathogenicity, and microbial competition. Thus, X. bovienii exemplifies the growing consensus that recombination not only maintains cohesion but can also allow the spread of niche-beneficial alleles.

Project description:Advances in sequencing technologies have accelerated our understanding of the complex genetic network of organisms and genomic divergences that are linked to evolutionary processes. While many model organisms and laboratory strains have been sequenced, wild populations are underrepresented in the growing list of sequenced genomes. Here, we present a de novo assembly of Steinernema feltiae, strain NW, collected from a working agricultural field in south central Washington, USA. Leveraging Pacific Biosciences (PacBio) long reads, we sequenced strain NW to a high depth (99×). The resulting de novo assembly is significantly larger than the previous assembly generated from the laboratory strain SN, with a noticeable improvement in continuity and completeness. Comparative analysis of two assemblies revealed numerous single nucleotide polymorphisms (SNPs), breakpoints, and indels present between the two genomes. This alternative genome resource and annotation could benefit the research community to examine the genetic foundation of evolutionary processes as well as genomic variation among conspecific populations.Advances in sequencing technologies have accelerated our understanding of the complex genetic network of organisms and genomic divergences that are linked to evolutionary processes. While many model organisms and laboratory strains have been sequenced, wild populations are underrepresented in the growing list of sequenced genomes. Here, we present a de novo assembly of Steinernema feltiae, strain NW, collected from a working agricultural field in south central Washington, USA. Leveraging Pacific Biosciences (PacBio) long reads, we sequenced strain NW to a high depth (99×). The resulting de novo assembly is significantly larger than the previous assembly generated from the laboratory strain SN, with a noticeable improvement in continuity and completeness. Comparative analysis of two assemblies revealed numerous single nucleotide polymorphisms (SNPs), breakpoints, and indels present between the two genomes. This alternative genome resource and annotation could benefit the research community to examine the genetic foundation of evolutionary processes as well as genomic variation among conspecific populations.

Dataset Information

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

Publications

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

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