Dataset Information

Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes.

ABSTRACT: Xenorhabdus bovienii (SS-2004) bacteria reside in the intestine of the infective-juvenile (IJ) stage of the entomopathogenic nematode, Steinernema jollieti. The recent sequencing of the X. bovienii genome facilitates its use as a model to understand host - symbiont interactions. To provide a biological foundation for such studies, we characterized X. bovienii in vitro and host interaction phenotypes. Within the nematode host X. bovienii was contained within a membrane bound envelope that also enclosed the nematode-derived intravesicular structure. Steinernema jollieti nematodes cultivated on mixed lawns of X. bovienii expressing green or DsRed fluorescent proteins were predominantly colonized by one or the other strain, suggesting the colonizing population is founded by a few cells. Xenorhabdus bovienii exhibits phenotypic variation between orange-pigmented primary form and cream-pigmented secondary form. Each form can colonize IJ nematodes when cultured in vitro on agar. However, IJs did not develop or emerge from Galleria mellonella insects infected with secondary form. Unlike primary-form infected insects that were soft and flexible, secondary-form infected insects retained a rigid exoskeleton structure. Xenorhabdus bovienii primary and secondary form isolates are virulent towards Manduca sexta and several other insects. However, primary form stocks present attenuated virulence, suggesting that X. bovienii, like Xenorhabdus nematophila may undergo virulence modulation.

SUBMITTER: Sugar DR

PROVIDER: S-EPMC3307839 | biostudies-literature | 2012 Apr

REPOSITORIES: biostudies-literature

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Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes.

Sugar Darby R DR Murfin Kristen E KE Chaston John M JM Andersen Aaron W AW Richards Gregory R GR deLéon Limaris L Baum James A JA Clinton William P WP Forst Steven S Goldman Barry S BS Krasomil-Osterfeld Karina C KC Slater Steven S Stock S Patricia SP Goodrich-Blair Heidi H

Environmental microbiology 20111212 4

Xenorhabdus bovienii (SS-2004) bacteria reside in the intestine of the infective-juvenile (IJ) stage of the entomopathogenic nematode, Steinernema jollieti. The recent sequencing of the X. bovienii genome facilitates its use as a model to understand host - symbiont interactions. To provide a biological foundation for such studies, we characterized X. bovienii in vitro and host interaction phenotypes. Within the nematode host X. bovienii was contained within a membrane bound envelope that also en ...[more]

PMID: 22151385

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Project description:Three bacterial strains, XENO-2T, XENO-7T, and XENO-10T, isolated from Steinernema entomopathogenic nematodes, were found to represent novel Xenorhabdus species. In this study, we describe these new species by whole-genome and whole-proteome phylogenomic reconstructions, by calculating sequence identity scores using core genome sequences, and by phenotypic characterization. Phylogenomic reconstructions using ribosomal and house-keeping genes, and whole-genome and whole-proteome sequences show that XENO-2T and XENO-10T are closely related to Xenorhabdus japonica DSM 16522T and that XENO-7T is closely related to Xenorhabdus bovienii subsp. africana XENO-1T and to X. bovienii subsp. bovienii T228T. The dDDH values between XENO-2T and XENO-10T and between XENO-2T and X. japonica DSM 16522T are 56.4 and 51.8%, respectively. The dDDH value between XENO-10T and X. japonica DSM 16522T is 53.4%. The dDDH values between XENO-7T and X. bovienii subsp. africana XENO-1T and between XENO-7T and X. bovienii subsp. bovienii T228T are 63.6 and 69.4%, respectively. These dDDH values are below the 70% divergence threshold for prokaryotic species delineation. The newly described species are highly pathogenic to G. mellonella larvae, grow at pH between 5 and 9 (optimum 5-7), at salt concentrations of 1-3% (optimum 1-2%), and temperatures between 20 and 37 °C (optimum 28-30 °C). Biochemical tests such as lysine decarboxylase, ornithine decarboxylase, urease, gelatinase, citrate utilization, indole and acetoin production, and cytochrome oxidase tests allow to differentiate the novel species from their more closely related species. Considering these genetic and phenotypic divergencies, we propose the following new species: Xenorhabdus aichiensis sp. nov. with XENO-7T (= CCM 9233T = CCOS 2024T) as the type strain, Xenorhabdus anantnagensis sp. nov., with XENO-2T (= CCM 9237T = CCOS 2023T) as the type strain, and Xenorhabdus yunnanensis sp. nov., with XENO-10T (= CCM 9322T = CCOS 2071T) as the type strain. Our study contributes to a better understanding of the biodiversity and phylogenetic relationships of entomopathogenic bacteria associated with insect parasitic nematodes.

Project description:Four Gram-stain-negative bacterial strains, CS20T, AUT15.5T, XENO-11T, and CCN3.3T, isolated from Steinernema entomopathogenic nematodes, were found to represent novel species within the genus Xenorhabdus (Gammaproteobacteria, Morganellaceae). In this study, we described these new species using whole-genome phylogenomic reconstructions, sequence identity values from core genome sequences, and phenotypic characterization. Phylogenetic reconstructions based on 16S rRNA gene sequences showed that: (i) strain CS20T is closely related to X. stockiae DSM 17904T, (ii) strain AUT15.5T is closely related to X. budapestensis DSM 16342T, (iii) strain XENO-11T is closely related to X. khoisanae DSM 25463T, and (iv) strain CCN3.3T is closely related to X. griffiniae DSM 17911T. The 16S rRNA gene sequence similarity value between strain CS20T and X. stockiae DSM 17904T is 97.8%, between strain AUT15.5T and X. budapestensis DSM 16342T is 98.1%, between strain XENO-11T and X. khoisanae DSM 25463T is 97.8%, and between strain CCN3.3T and X. griffiniae DSM 17911T is 98.6%. Phylogenomic reconstructions using whole-genome sequences showed that: (i) strain CS20T is closely related to X. stockiae DSM 17904T and X. innexi DSM 16336T, (ii) strain AUT15.5T is closely related to X. indica DSM 17382T, (iii) strain XENO-11T is closely related to X. khoisanae DSM 25463T, and (iv) strain CCN3.3T is closely related to X. griffiniae DSM 17911T. The digital DNA-DNA hybridization (dDDH) and average nucleotide identity (ANI) values between strains CS20T, AUT15.5T, XENO-11T, and CCN3.3T and the type strains of their more closely related species are below the 70% and the 95-96% divergence thresholds, respectively, used for prokaryotic species delineation. Hence, we propose the following four new species: Xenorhabdus bharatensis sp. nov. (the type strain is CS20T=CCM 9320T=CCOS 2070T), X. entomophaga sp. nov. (the type strain is XENO-11T=CCM 9389T=CCOS 2111T), X. siamensis sp. nov. (the type strain is AUT15.5T=CCM 9405T=CCOS 2116T), and X. thailandensis sp. nov. (the type strain is CCN3.3T=CCM 9406T=CCOS 2115T). The following biochemical tests may be useful for differentiating the novel species from their more closely related taxa: acetoin production, arginine dihydrolase, citrate utilization, gelatinase, glucose oxidation, indole production, and tryptophan deaminase. Our study contributes to a better understanding of the biodiversity and phylogenetic relationships of entomopathogenic bacteria associated with insect parasitic nematodes.

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.

Dataset Information

Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes.

Publications

Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes.

Similar Datasets

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